Neural Crest: Contributions to the Development of the Vertebrate Head

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Neural Crest: Contributions to the Development of the Vertebrate HeadAuthor(s): Ann C. GravesonSource: American Zoologist, Vol. 33, No. 4 (1993), pp. 424-433Published by: Oxford University Press

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Amer.

Zool.,

33:424-433

(1993)

Neural

Crest:

Contributions

to

the

Development

of the

Vertebrate Head1

Ann C. Graveson

Department of Biology, Dalhousie University, Halifax, Nova Scotia B3H 4J1, Canada

Synopsis. The

neural

crest

is

a

major

source

of

mesenchyme

in

the

head,

but

not the

body,

of the vertebrate

embryo.

For some

of

these mesen-

chymal

derivatives,

the differences between

the

normal

fates of cranial

and trunk neural crest cells are

not

necessarily

due

to

differences

in

the

potentials

of

the cells for the

various

derivatives,

but reflect

a

lack

of

interaction

with

appropriate

inductive tissues.

Chondrogenic

potential,

however,

is restricted to those

axial levels

which

normally

give

rise

to

cartilage.

This

chondrogenic

subpopulation

is

not

homogeneous;

even

prior

to neural crest cell

migration,

cells from different axial

levels

display

differences in

migratory

and

morphogenetic

abilities.

While the

events

which

give

rise

to

these

segregations

have

never

been

examined,

some

models have been

proposed

for

the establishment

ofthe

neural

crest

itself.

Introduction

In

this

review,

I will

discuss

only briefly

the

basic

roles and

functions

of

neural

crest,

and direct the

reader to the

more

detailed

accounts of Weston

(1970),

LeDouarin

(1982), and Hall andH6rstadius(1988). This

paper

deals

with various

aspects

of,

and

assumptions about,

the

mesenchymal

derivatives of these

cells,

which

not

only

play

a

major

role

in

the

development

ofthe

vertebrate

head,

but whose

production

is

often considered

a

characteristic

of

head,

but not

trunk,

neural

crest.

Despite

its broad role

in

vertebrate devel?

opment,

there is no

simple

definition ofthe

neural

crest. The

only

satisfactory

defini-

tions

are

functional: where

the cells

arise,

how

they

behave,

and their

ultimate fates.

Thus,

the

neural

crest consists of

those cells

which have

combinations of

the

following

characteristics,

none

of

which

alone

is

suf?

ficient to

define

the neural

crest:

i)

The

cells are

initially

found in

the

neu?

ral

folds,

at

the

boundary

between

the

neural

plate

(neurectoderm)

and the

non-neural

(epidermal)

ectoderm.

However,

not all cells

1

From the

Symposium

on

Development

and

Evo?

lution

ofthe

Vertebrate

Head

presented

at the

Annual

Meeting

ofthe

American

Society

of

Zoologists,

27-30

December

1991,

at

Atlanta,

Georgia.

within the neural

folds

are

neural crest

cells;

neural

folds also contain

presumptive

brain

and

epidermal

cells

(Brun,

1984,

1985).

Furthermore,

neural

crest cells can also

arise

outside

the

neural

folds,

both

from the neu?

ral plate and from adjacent ectoderm (Brun,

1981, 1985;

Lumsden,

1988).

In

the

head,

this

adjacent

ectoderm

is

placodal,

and

will

give

rise

to the sense

organs,

and

some of

the cranial

ganglia.

Placodal ectoderm

is

considered

to be distinct

from the

neural

crest,

despite

some similarities

in

behaviour

and

derivatives,

and

is

discussed

by

Webb

and

Nolan

(1993).

ii)

Neural crest

cells

do

not

remain

in

the

neural

tube.

At some

stage,

usually

after,

but in some

species

before,

neural tube clo?

sure,

they begin

an extensive

migration along

specific

pathways

to

their

ultimate

desti-

nations.

They

do

not

emigrate

at the same

time

from

all axial levels

of

the

neurepi-

thelium;

migration usually begins

at the

mesencephalic

level,

and

progresses

both

anteriorly

and

posteriorly

from this

point.

In

those

mammals

which

have

been

stud?

ied,

however,

neural

crest

emergence

does

not follow this axial

sequence

(Morriss-Kay

andTan,

1987).

iii)

Finally,

neural crest cells

differentiate

into

a

wide

variety

of

cell

types,

among

which are

pigment

cells,

with the

exception

of those ofthe

pigmented

retina

(which

are

424







Neural Crest 425

formed

by

the

neural

plate),

and

the

ele?

ments of the

peripheral

nervous

system,

except

for some cranial

ganglia,

which are

derived from ectodermal

placodes.

Pigment

and neuronal

cells

can

and do arise

from all

axial levels of neural

folds,

both cranial

(adjacent

to

the

presumptive

brain)

and

trunk

(adjacent

to the

presumptive spinal

cord). Figure

1

depicts

the locations of these

axial levels

in

an

amphibian

neurula,

as well

as the

system

of

coordinates which

will

be

used

to describe the axial levels of cranial

neural folds.

Neural crest

cells also

give

rise to a

large

number of

mesenchymal

derivatives,

including cartilage, bone,

odontoblasts of

the

teeth,

and connective tissues. These

derivatives tend

to be considered as a

sep-

arate

class,

because all can also be derived

from

mesoderm,

except

the

odontoblasts,

and

because their

production

is

generally

considered to be the

domain of

cranial,

but

not

trunk,

neural crest.

However,

it must be

noted that while this

is

generally

true,

the

production

of

mesenchymal

cells is

not

exclusive

to the cranial

neural crest. For

example, in amphibians, the mesenchyme

ofthe

dorsal

fin

is

derived from

trunk neural

crest

(Hall

and

Horstadius,

1988).

Detailed

fate

maps

for the neural

crest are

available for

both

amphibians

and

birds,

where labelled cells

from different axial lev?

els

were followed to

the individual skeletal

elements.

Extirpations

of

segments

of

neu?

ral folds

from

lamprey

and teleost

embryos

have also

been

performed

to

identify

the

neural

crest-derived

skeletal

elements,

as

well as the axial levels from which

they

arise.

The

results are

remarkably

similar

in

all

species

studied to

date

(Hall

and

Horstad?

ius,

1988).

The entire

visceral

skeleton,

except

for the

second

basibranchial,

is neu?

ral

crest-derived.

Portions of the

neuro-

cranium are

also neural

crest-derived.

The

only

differences

among

the classes

appear

to be

in

some

elements

which are

mainly

of

mesodermal

origin.

For

example,

while

the

otic

capsule appears

to be

entirely

of

mesod?

ermal

origin

in

amphibians,

there is a

neural

crest cell

contribution

in

birds.

Conversely,

the avian

parachordal

and basal

plate

car?

tilages

are

entirely

derived

from

mesoderm,

although

there is a

nonessential neural

crest

Fig. 1.

System

of

coordinates

used to

describe the

axial

levels of

amphibian

cranial neural

folds,

shown

here on a

mid-neurula

stage

axolotl

embryo.

Cranial

neural

folds are

found at

levels

0?-150?,

while

trunk

neural

folds are at all

levels

posterior

to

150?.

Adapted

from

Chibon

(1966).

contribution

in

amphibians

(in

the

absence

of

neural crest

cells,

these

elements

will

develop

normally;

Chibon,

1966). Finally,

these

labelling

and

extirpation

studies have

also

demonstrated similar

regionalisations

ofthe

skeletogenic

neural

crest;

rostral skel?

etal elements

originate

from rostral

levels,

caudal

elements from more

caudal levels.

Unfortunately,

we do not

yet

have a

detailed

fate

map

for the mammalian neural

crest,

although

current

information tends to

sug?

gest

that it is

similar to other

vertebrates;

cranial

neural crest

cells have

skeletogenic

potential,

and their

migratory

pathways

not

only

lead them

to the

visceral

arches,

but

the

relationship

between

their

rostro-caudal

origin

and the

various arches

is similar

to

that seen

in

the other

classes

(Morriss-Kay

andTan,

1987).

Fate

Versus

Potential: Cartilage

Because of their

extensive

migration,

neural crest

cells have

ample

opportunity

to

contact and interact

with a

large

number of

cells,

tissues,

and

extracellular

matrices.

In







426

A. C. Graveson

fact,

these interactions

are essential

for the

proper

differentiation

of skeletal

tissues

in

all

species

studied

to date.

However,

the

inductive

tissue is not

always

the same.

In

amphibians,

chondrogenesis

from

neural

crest

cells

always

requires

an

inductive

interaction

with

pharyngeal

endoderm.

In

some

species,

such as the

axolotl

(Ambys?

toma

mexicanum;

Graveson and

Arm-

strong, 1987)

and Triturus

alpestris

(Epper-

lein and

Lehmann,

1975),

this is

sufficient,

but

in

others there are

additional

require-

ments,

such

as dorsal mesoderm

for Pleu-

rodeles waltl

(Corsin,

1975),

or stomodeal

ectoderm

for

Ambystoma

maculatum

(Wilde, 1955). For the chick, the inductive

tissue is ectoderm.

It is not known

if

these

different

tissues are

producing

the same or

different

signals,

but cranial

neural crest from

lampreys

can be induced

to

chondrify using

amphibian

head

epithelia

as the

inductor

(Newth,

1956).

Pharyngeal

endoderm is the

only

induc?

tor

required

for

chondrogenesis

ofthe neu?

ral crest

in

the axolotl

(Graveson

and

Arm-

strong, 1987).

We have shown that all the

endoderm of the head is equally inductive,

but that neither trunk

endoderm

nor noto-

chord

(which

is the inductor for somitic

chondrogenesis)

has

any

inductive

capacity.

Given

that

chondrogenesis

requires

con?

tact with

endoderm,

and that inductive abil?

ity

is found

exclusively

in

the

head,

it is

possible

that the

trunk neural crest does not

form

cartilage

because it never comes into

contact with the inductive

endoderm under

normal

circumstances.

Therefore,

while the

trunk

neural crest is

not fated to form car?

tilage,

the

question

arises as to whether it

has

the

potential

to do so. This

question

has

been asked

before,

but the

potential

of the

neural

crest has

usually

been tested

by

trans-

planting

trunk neural

crest into the head.

There is a

basic

assumption

underlying

this

approach:

that the

transplanted

trunk neu?

ral crest

cells are

thereby

exposed

to all

of

the

inductive

influences

that head neural

crest cells normally encounter. However, this

assumption

has now

been shown to

be

untrue.

For

example,

in

the

axolotl,

after the

pre?

sumptive

chondrocytes

of

the

branchial

arches leave

the

neural

tube,

they

initially

migrate

between the ectoderm

and the

mesoderm

(Fig.

2A,

B),

then move into the

branchial

arches,

surrounding

the

mesoder-

mal core

(Fig. 2C),

and

finally

contact the

pharyngeal

endoderm

while

continuing

their

ventral

migration (Fig. 2D) (Stone, 1922).

However,

when trunk neural folds are

transplanted

to cranial

levels,

the trunk neu?

ral crest cells do not follow the cranial

migration pathways (Fig. 3).

In

fact,

there

appears

to be

very

little

migration,

except

for a few

pigment

cells

(Fig. 3B).

Therefore,

transplanting

trunk neural crest

cells to the

appropriate

cranial level

will

not

necessarily

test their

potential

for

chondrogenesis;

the

cells cannot follow head migration path?

ways

and thus cannot contact the inductive

endoderm,

at least

in

the

axolotl.

Since the

chondrogenic

potential

of trunk

neural crest cells

could not be tested

using

heterotopic transplantations,

its

potential

was

directly

tested

by

placing

it

in

intimate

contact with

inductive endoderm

in

explant

culture.

Under these

conditions,

>90?/o of

cultures

containing

cranial neural

crest form

cartilage (Graveson

and

Armstrong,

1987).

Explants containing trunk neural crest never

formed

cartilage.

Trunk neural crest there?

fore does not

have

chondrogenic

potential,

fortuitously confirming

the

conclusions

based on

transplantation experiments

(Chi?

bon,

1966;

Hall

and

Horstadius,

1988).

The anterior-most

neural

folds,

known

as

the

transverse

fold

in

amphibians

(0?-30?;

Fig. 1),

is

also

normally

non-skeletogenic.

Indeed,

it is often

considered not to

contain

neural

crest cells at

all,

but to

only

form

part

of the

forebrain.

Again,

the lack

of chon?

drogenesis

may

be due to

a lack of

potential

or to a lack

of interaction

with an

inductive

tissue,

a

problem

that

remains

unresolved.

Although

we have

never had

cartilage

develop

from

cultures of

transverse fold and

inductive

endoderm

in

the

axolotl,

cartilage

has been

reported

to

develop

in

explant

cul?

tures from

another

urodele,

Pleurodeles waltl

(Cassin

and

Capuron,

1979),

and two

anu?

rans (Xenopus laevis; Seufert and Hall, 1990;

and

Discoglossus

pictus;

Cusimano-Carollo,

1972).

This

may

reflect

species

differences

or

some other

factors,

such as

differences

in

the

tissues

used,

or

different

culture con?

ditions.







Neural

Crest 427

Fig. 2. Normal

migration patterns

of cranial

neural crest

in

A. mexicanum.

A

cranial neural fold

(80?-150?;

Fig.

1)

was

homotopically

transplanted

from a

wild-type

to an albino neurula. The neural

crest cells can be

visualized

through

the

pigmentless

ectoderm ofthe host. See text

for

details.

m:

mandibular;

h:

hyoid;

b: branchial.

Bar

=

1

mm.

Adapted

from Graveson

(1990).

Thus,

it

appears

that,

for the axolotl at

least,

the

only

neural

crest which has chon-

drogenic

potential

is that which

normally

contributes to the

skeleton

(30?-150?).

In

this

case, potential equals prospective

fate.

Fate

Versus

Potential:

Teeth

and Fin

Mesenchyme

It is

important

to

note, however,

that the

normal fate of cells is not

always

a reflection

of their

potential.

One

case

in

point

is

that

of another

derivative of

the cranial neural

crest,

the

odontoblasts,

which

produce

the

dentine ofthe teeth.

Chibon

(1966),

in

map?

ping

the

cartilaginous

neural crest

elements

in Pleurodeles waltl, also mapped the origin

of the

teeth

using

heterotopic transplants.

He showed that the

odontoblasts are

derived

from the same axial

levels of neural

folds

as the skeletal

elements which

support

them.

The

palatine

teeth arise from the folds

between

30? and

70?,

and the mandibular

teeth from

those between

70?

and 100?. The

fate

map

for odontoblasts therefore com-

prises

the levels from

30?

to

100?,

which is

much less than

that

for

the

chondrogenic

levels,

which extend from 30? to 150?. Based

on the

results of his

transplantations

of

labelled

posterior

cranial and trunk neural

folds to

normally odontogenic

levels,

Chi-

bon

(1966)

concluded that the neural crest

cells from these levels did not have odon?

togenic

potential,

although

1

of

his

30 trunk

transplantations

did

give

rise to labelled

odontoblasts.

Like

chondrogenesis,

tooth formation is

also the result of a series of tissue interac?

tions.

Although

the

parameters

ofthe induc-

tion(s)

are not

completely

known

in

amphibians,

we

have

developed

an

explant

culture

system

which

produces

teeth

in

the

majority

of

cases,

when cranial neural

crest







428

A.

C.

Graveson

Fig.

3.

Lack

of

migration

of trunk

neural

crest

following

transplantation

to cranial levels. A

trunk neural

fold

from

a

wild-type

neurula was

transplanted

to levels

80?-150?

(Fig. 1)

of an albino

neurula. The

embryos

in

A

and B

were at the

same

stages

as those

in

Figure

2A

and

C,

respectively.

Bar

=

1

mm.

Adapted

from

Graveson

(1990).







Neural Crest

429

from

30?-100? is included.

Using

this

sys?

tem,

we are

testing

the

odontogenic

poten?

tial

of neural crest cells

from different

axial

levels.

Although

we

only

have

preliminary

results at this

time,

it

appears

that

odon?

togenic

potential

is much

more extensive

than

previously

suspected.

In

fact,

the

odontogenic

potential

of the

neural crest

appears

to

extend even

further

posteriorly

than

the

chondrogenic

potential.

While cul?

tures

containing

inductive

endoderm

and

cranial neural crest

from known chondro?

genic

levels

develop

both

cartilage

and

teeth,

there is a short

segment

immediately

pos?

terior to

150?

from which teeth

develop,

but

cartilage does not (Graveson, M. M. Smith,

and

Hall,

in

preparation).

Lumsden

(1988)

has

reported

similar results with

cultures of

mouse

trunk

neural crest cells and

inductive

epithelia,

in

which both teeth and bone are

formed.

There

is,

therefore,

a

long

segment

of

neural crest whose

odontogenic

potential

is

not

normally

realized

due

to an

apparent

lack of interaction with

the

appropriate

inductive

tissues;

fate does not

equal

poten?

tial for

the

odontogenic

neural crest.

This is also true for a number of other

neural

crest derivatives. The

dorsal

fin

of

amphibians

is

the

result of an

interaction

between trunk

neural crest

and

the

overly-

ing

epidermal

ectoderm.

Amphibians

do not

have a

fin

on the

head,

but

this is not

because

of

differences

in

the

potential

of cranial and

trunk

neural

crest,

but because head

ecto?

derm

cannot

participate

in

dorsal

fin

for?

mation

(Woerdeman,

1946).

Similarly,

in

the

chick,

where

only

cranial

neural crest

normally

forms

mesenchymal

derivatives,

it has been shown

that

early

trunk neural

crest can form

dermis

and

connective

(though

not

skeletal)

tissue,

given

the

right

conditions

(Nakamura

and

Ayer-LeLievre,

1982).

These

studies

demonstrate that when

the

potentials

rather than

fates ofthe

neural

crest

cells

are

considered,

there does

not

appear

to be

an

absolute

distinction

between

cra?

nial and trunk, with the possible exception

ofthe

chondrogenic subpopulation

(Fig. 4).

The

localization

of derivatives

depends

not

only

on the

potential

of these

cells,

but

also

on

the

presence

of

the

inductive

tissues

required

to

elicit this

potential.

FATE

POTENTIAL

Fig. 4.

Comparison

of

axial levels

of

neural crest cells

which

normally produce specific mesenchymal

deriv?

atives

(left)

with

the axial levels

of

neural

crest which

have

the

capacity

to

form them

(right),

in

the axolotl.

The horizontal line delineates the cranial and trunk

levels of neural folds

(150?).

F:

dorsal

fin

mesenchyme;

O:

odontoblasts;

C:

chondrocytes.

Regionalisation

of

the

Cranial

Neural Crest

The results

of

heterotopic

transplanta-

tions,

while not

necessarily

useful

for

testing

potential,

clearly

demonstrate

that cells

with

the same potential are not identical (see also

Langille,

1993).

There

appears

to

be a

regionalisation

within

the cranial

neural crest

which is

present

prior

to

the onset of cell

migration.

Posterior

cranial neural crest did

not

participate

in

tooth formation when

transplanted

to anterior cranial levels

although

the

cells

have

odontogenic

poten?

tial and were

placed

at axial levels whose

migration

routes

normally

lead to inductive

tissues.

Therefore,

these cells must differ at

least

in

their

ability

to

follow

different

migration pathways. Similarly,

branchial

arch

crest cells

will

not form

any

skeletal

elements when

transplanted

to the level

of

the anterior trabecular crest

(Chibon,

1966).

Differences

in

the

ability

to

follow

migra?

tion

cues

are

not

the

only

differences

pres?

ent,

however.

Horstadius described 3 dis?

tinct

levels

of

chondrogenic

neural

crest,

based

on

heterotopic transplantations

in

the

axolotl: trabecular (30?-70?), mandibular

(70?-100?),

and

branchial

(100M500)

(Hall

and

Horstadius,

1988).

The

trabecular neu?

ral

crest cannot form

any

of

the

visceral

arches,

while visceral

arch

crest

cannot

form

trabeculae. This

may

be

the result of

differ-







430

A.

C.

Graveson

ences

in

migratory

abilities,

as described

previously. Finally,

the mandibular

and

branchial

arch levels also

appear

to

be dis-

tinct,

although

not

because

of

migratory

dif?

ferences. Heterotopically transplanted neu?

ral crest cells

will

follow the

appropriate

route for the new

level,

and

will

differentiate

into arch

elements,

but the elements

formed are not

completely

normal.

The car?

tilages

derived from branchial levels

always

fuse with

the

basibranchials,

even when

they

are at mandibular levels.

Conversely,

the

elements derived

from mandibular levels

never fuse with the basibranchials

when

placed

at branchial

levels;

they

remain free.

The cells from a particular level do not

appear

to

have

a

fixed

fate,

but

rather,

seem

to have a limited

range

of

possible

mor?

phological

fates,

with

the ultimate

element

produced

being

influenced

by

the local

envi?

ronment.

In

the

chick,

there

appears

to

be

an

early regionalisation

of neural

crest

cells

destined to form the

visceral arch

elements,

while

they

are still

in

the

neural folds. Het?

erotopically

transplanted

neural crest cells

apparently

follow

the normal

migratory

route for the new axial

level,

and differen?

tiate into the

appropriate

tissue,

but the

type

of element which is

formed is not neces-

sarily

appropriate

for

either the

new or

the

original

location;

neural crest

from levels

destined to form

frontonasal

structures

gave

rise to

mandibular elements

when trans?

planted

to

the

hyoid

level,

after

migrating

to the

hyoid

arch

(Noden, 1988).

The

pos?

sibility

that neural crest

cells

may

possess

a

range

of

morphological

fates is borne

out

by

Chibon's

(1966)

observations of

regu?

lation

following

neural crest

extirpation

in

Pleurodeles

waltl;

bilateral removal of

seg?

ments less

than

30? resulted

in

complete

reg?

ulation,

leading

to

normal

skeletogenesis.

The

replacement

cells

must have been

derived

from

flanking segments

of

neural

crest

cells;

if

the

missing

cells

were

replaced

by

new

neural

crest

cells,

regulation

would

also be

possible

for

longer

extirpations,

which was not the case.

In

summary,

there are

three

ways

in

which

chondrogenic

neural crest

can be shown

to

be

segregated.

Each of

these

successively

subdivides

the

cells into

smaller

subpopu-

lations.

The

first is

the

restriction

of

chon-

drogenic

potential

to

only

those axial

levels

which are

normally chondrogenic.

The

sec?

ond

is the

restriction

of

migratory

abilities,

and the

third

is the

restriction of

morpho?

genetic potential.

This

regionalisation

within the

cranial

neural

crest stands

in

stark

contrast

to the

results

of similar

studies of

heterotopic

transplantations

within

amphibian (Chi-

bon,

1966)

and chick

(LeDouarin,

1982)

trunk

neural

crest,

where

the

neural

crest

cells

apparently migrate

and differentiate

completely

in

accordance

with their

new

locations.

Neural Crest Formation

Thus

far,

I

have

concentrated

on the

chondrogenic

neural

crest,

since it

is a

strictly

cranial

derivative

(with

respect

to both

its

fate

and

potential),

plays

a

major

role

in

the

development

ofthe

vertebrate

head,

and is

an

extremely

well-studied

system.

We have

yet

to determine

how

potential

becomes restricted

to cranial

levels. Do

all

neural

crest cells

initially

have chondro?

genic ability

which is

subsequently

lost from

trunk cells?

Or are all neural

crest cells

ini?

tially non-chondrogenic

with those

in

the

head

subsequently acquiring

this

potential?

As a final

possibility,

perhaps

cranial and

trunk neural crest

are

truly

distinct,

arising

via

different

processes.

These

questions

have

never been addressed.

This is not

surprising,

since the

processes

responsible

for

neural

crest formation

per

se are not

known. This

question,

at

least,

has been

addressed,

but

there is

no

definitive answer.

It is

generally

believed that

neural crest

formation is associated with neural

induc?

tion,

when

the chordamesoderm

(the

future

notochord and

adjacent

mesoderm)

induces

the

overlying

ectoderm

to

neuralise and

acquire anterior/posterior

regionalisation

properties.

Neural crest would arise either

as

a direct result of neural

induction,

or as

the result of a

process

immediately

subse?

quent

to it. Several models have been

pro?

posed (Fig. 5), each of which is supported

by

different

experimental

evidence. Since

most

of the

experimental

evidence

was

obtained

using

the

axolotl,

species

differ?

ences cannot

account

for the

differences

in

the models.







Neural

Crest 431

In

one

model,

proposed by

Raven

and

Kloos

(1945,

1946;

Fig.

5A),

neural crest is

formed because

of

differences

in

the induc-

ing

tissues. The

inductive field

of

chorda-

mesoderm is

presumed

to be rather

broad,

and there are

quantitative

differences

in

the

putative

signal

between

the medial and

lat?

eral

portions

of

the

chordamesoderm.

The

response

of the

ectoderm

depends

on the

quantity

of

signal;

high

signal

levels

give

rise

to mid-neural

plate,

and low to

neural crest.

In

another model

(Nieuwkoop

et

al,

1985;

Albers, 1987;

Nieuwkoop,

1985;

Fig.

5B),

neural crest

is

formed because

of

differences

in

the

responding

tissues. The inductive

chordamesoderm consists mainly or solely

of

presumptive

notochord,

which induces

only

the ectoderm

directly overlying

it

(the

mid-neural

plate).

After this initial

step,

neural induction

proceeds

homiogeneti-

cally;

neuralised ectoderm induces

adjacent

ectodermal cells

to

neuralise,

and

the

signals

are

then

propagated through

the ectoderm

itself. With

time,

the

competence

of the

ectoderm to

respond

to

the induction fades.

Neural crest is the result of a weakened

response,

caused

by

the loss of

competence.

In

the

indirect models

(Fig.

5C,

D),

neural

crest formation is

believed

to be

the result

of

interactions between

the

products

of neu?

ral induction.

In

other

words,

the neural

crest is

formed at

the

junction

between neu?

ral and non-neural

ectoderm because these

tissues are

apposed.

Moury

and

Jacobson's

(1990)

model

(Fig.

5C) requires

only

the

presence

of

ectoderm next to

neurectoderm,

but

Rollhauser-ter-Horst

(1977a, b, 1979)

believes

that neural

crest formation

requires

the

presence

of

additional, unidentified,

tis-

sue(s)

(Fig. 5D).

However,

the

question

of

anterior/pos-

terior

regionalisation

of the

neural crest is

not

addressed

by any

of these models. One

ofthe

major

stumbling

blocks

has been that

the

number of

steps

involved has not been

determined,

possibly

because

specification

and

regionalisation

of

the neural

crest

(if

there is more than a single step involved)

occur

in

rapid

succession.

However,

we think

that

we

may

have a useful model

for

study-

ing

this

(these)

process(es),

in

the

form

ofa

developmental

mutant

of

the

axolotl.

This

mutation,

aptly

named

premature

death

(p),

Direct

tefeH

*

B

-

Subsequent

c

H^*V I l

Qj

Fig.

5. Models for neural crest formation.

A

and

B:

neural crest formation as

a

direct

result of

neural induc?

tion;

C and

D:

neural crest

formation as

a

result

of

interactions

occurring

subsequent

to

neural induction.

See text for details.

affects

some,

but not

all,

neural crest

cells,

including

the

chondrogenic

subpopulation

(Graveson

and

Armstrong,

1990,

in

prep?

aration).

The mutant

gene

affects

the

ecto-

derm;

chordamesoderm,

whatever

its

role,

is

apparently

normal

(Graveson

and

Arm?

strong,

in

preparation).

We

suspect

that

an

early segregation event is affected. Neural

crest

cells are

established,

and

appear

to be

properly regionalised

with

respect

to

their

migratory

ability

along

specific pathways

at

specific

axial

levels,

but these

apparently

normal

neural crest

cells

appear

to be

inca-







432

A. C. Graveson

pable

of

normal differentiation.

Particularly

exciting

is our

recent

finding

that the lateral-

line

placodes,

which arise

in

the head ecto-

derm

immediately adjacent

to the

neural

folds, are also affected by the p gene (Grave?

son,

S. C.

Smith,

and

Hall,

in

preparation).

This

strongly suggests

the

presence

of a

developmental

(and

possibly

evolutionary)

link,

which

has

long

been

suspected,

between

the neural crest

and

ectodermal

placodes.

Acknowledgments

This work

was

supported by

operating

grants

to

J.

B.

Armstrong

and

B. K. Hall

from

the Natural Science

and

Engineering

Council of Canada. I thank B. K. Hall and

S.

C. Smith

for their

valuable comments

and

discussions.

References

Albers,

B.

1987.

Competence

as

the main factor

determining

the size

of the neural

plate.

Dev.

Growth

Differ. 29:535-545.

Brun,

R.

B.

1981.

The movement

of the

prospective

eye

vesicles

from

the neural

plate

into

the neural

fold

in

Ambystoma

mexicanum

and

Xenopus

lae-

vis. Dev. Biol. 88:192-199.

Brun,

R. B. 1984.

Mapping

the neural crest cells

in

the Mexican

salamander

(Ambystoma

mexi?

canum).

Amer. Zool. 24:A100.

Brun,

R.B. 1985. Neural

fold and neural

crest

move?

ment

in the Mexican salamander

Ambystoma

mexicanum.

J.

Exp.

Zool.. 234:57-61.

Cassin,

C.

and

A.

Capuron.

1979. Buccal

organogen-

esis

in

Pleurodeles

waltlii

Michah

(urodele

amphibian). Study

in

intrablastocoelic

transplan-

tation

and in vitro culture.

J.

Biol. Buccale

7:61?

76.

Chibon,

P. 1966.

Analyse

experimentale

de

la

region?

alisation et des

capacites morphogenetiques

de la

crete neurale chez

Pamphibien

urodele

Pleurodeles

waltlii Michah. Mem.

Soc. Zool.

Fr.

36:1-107.

Corsin,

J.

1975. Differentiation

in vitro

de

cartilage

a

partir

des

cretes

neurales

cephaliques

chez Pleu?

rodeles waltlii

Michah.

J.

Embryol.

Exp.

Morphol.

33:335-342.

Cusimano-Carollo,

T. 1972. On the

mechanism of

the formation ofthe larval

mouth

in

Discoglossus.

Acta

Embryol.

Exp.

4:289-332.

Epperlein,

H. H. and

R. Lehmann. 1975.

The ecto-

mesenchymal-endodermal

interaction

system

(EEIS)

of

Triturus

alpestris

in

tissue

culture. 2.

Observations

on the differentiation

of visceral car?

tilage.

Differentiation

4:159-174.

Graveson,

A. C. 1990. Studies

on

the

differentiation

of

cranio-visceral

cartilage

in

normal

and

pre-

mature death

mutant

embryos

of

Ambystoma

mexicanum. Ph.D.

Thesis,

University

of

Ottawa,

Ottawa.

Graveson,

A.

C and

J.

B.

Armstrong.

1987.

Differ?

entiation of

cartilage

from cranial neural crest

in

the axolotl

(Ambystoma

mexicanum).

Differenti?

ation 35:16-20.

Graveson,

A.

C and

J.

B.

Armstrong.

1990.

The

premature death (p) mutation of Ambystoma mex?

icanum affects a

subpopulation

of

neural crest

cells.

Differentiation 45:71-75.

Hall,

B. K. and

S.

Horstadius.

1988.

The neural crest.

Oxford

University

Press,

London.

Langille,

R.

M. 1993. Formation

ofthe vertebrate

face. Amer. Zool.

33:462^171.

LeDouarin,

N. M.

1982. The neural

crest.

Cambridge

University

Press,

Cambridge.

Lumsden,

A. G. S. 1988.

Spatial

organization

ofthe

epithelium

and the role of neural crest cells

in

the

initiation of the mammalian tooth

germ.

In P.

V.

Thorogood

and C. Tickle

(eds.), Craniofacial

development, Development, Vol. 103 (suppl.), pp.

155-169. The

Company

of

Biologists

Ltd.,

Cam?

bridge.

Morriss-Kay,

G.

and

S.-S.

Tan. 1987.

Mapping

cra?

nial

neural

crest

cell

migration pathways

in

mam?

malian

embryos.

Trends Genet. 3:257-261.

Moury,

J.

D. and

A.

G.

Jacobson.

1990. The

origins

of

neural crest cells

in the

axolotl. Dev.

Biol. 141:

243-253.

Nakamura,

H. and

C. S.

Ayer-LeLievre.

1982.

Mesectodermal

capabilities

ofthe trunk neural crest

of

birds.

J..

Embryol.

Exp.

Morphol.

70:1-18.

Newth,

D. R. 1956. On the neural crest ofthe

lamprey

embryo. J. Embryol. Exp. Morphol. 4:358-375.

Nieuwkoop,

P. D. 1985. Inductive

interactions

in

early

amphibian

development

and their

general

nature.

J.

Embryol.

Exp. Morphol.

89(suppl.):333-

347.

Nieuwkoop,

P.

D.,

A.

G.

Johnen,

and B. Albers. 1985.

The

epigenetic

nature

of early

chordate

develop?

ment.

Cambridge University

Press,

Cambridge.

Noden,

D.

M.

1988. Interactions and fates of

avian

craniofacial

mesenchyme.

In P. V.

Thorogood

and

C.

Tickle

(eds.), Craniofacial

development,

Devel?

opment,

103

(suppl.), pp.

121-140.

The

Company

of

Biologists

Ltd.,

Cambridge.

Raven,

C.

P. and

J.

Kloos. 1945. Induction

by

medial

and lateral

pieces

of

the archenteron

roof,

with

special

reference to the determination ofthe neural

crest. Acta Neerl.

Morphol.

5:348-362.

Raven,

C. P.

and

J.

Kloos.

1946. Induction

by

medial

and

lateral

parts

of the

archenteron

roof;

deter?

mination ofthe neural crest. In M. W.

Woerdeman

and

C. P.

Raven

(eds.),

Experimental

embryology

in

the

Netherlands,

1940-1945. Elsevier

Publish?

ing

Co., Inc,

New

York.

Rollhauser-ter

Horst,

J.

1977a.

Artificial neural

induction

in

amphibia.

I.

Sandwich

explants.

Anat.

Embryol.

151:309-316.

Rollhauser-ter

Horst,

J.

19776. Artificial neural

induction

in

amphibia.

II. Host

embryos.

Anat.

Embryol.

151:317-324.

Rollhauser-ter

Horst,

J.

1979.

Artificial neural crest

formation

in

amphibia.

Anat.

Embryol.

157:113-

120.

Seufert,

D.

W.

and B.

K. Hall.

1990. Tissue

inter-







Neural

Crest

433

actions

involving

neural crest

in

cartilage

forma?

tion

in

Xenopus

laevis

(Daudin).

Cell

Diff.

Devel.

32:153-166.

Stone,

L. S. 1922.

Experiments

on

the

development

of the

cranial

ganglia

and the lateral line sense

organs

in

Amblystoma punctatum.

J.

Exp.

Zool.

35:421-496.

Webb,

J.

F. and D. M.

Noden. 1993. Ectodermal

placodes:

Contributions to

the

development

ofthe

vertebrate

head. Amer. Zool. 33:434-447.

Weston,

J.

A.

1970. The

migration

and differentia-

tion of

neural crest

cells. Adv.

Morphogen.

8:41?

114.

Wilde,

C

E.

1955. The

urodele

neuroepithelium.

I.

The

differentiation in

vitro of the

cranial

neural

crest.

J.

Exp.

Zool.

130:573-595.

Woerdeman,

M. W.

1946.

Induction of

dorsal fins

by

neural crest in

Amblystoma

mexicanum.

In M.

W.

Woerdeman and C P.

Raven

(eds.), Experi?

mental

embryology

in the

Netherlands,

1940-1945,

pp.

15-18.

Elsevier

Publishing

Co., Inc,

New

York.

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