Radioautographic study of the axonal transport of proteins into the sensory nerve endings of avian mechanoreceptors

0306-4522~83 010133-10$0;03.00’0 Peigomon Press Ltd iBKO

RADIOAWTOGRAPHIC STUDY OF THE AXONAL TRANSPORT OF PROTEINS INTO THE SENSORY NERVE ENDINGS OF AVIAN MECHANORECEPTORS C. N. CHWJCHKOV, D. V. MARKOV* and G. P. GALABOV Department of Anatomy. Histology and Embryology Medical Academy and *Regeneration Research Laboratory, Bulgarian Academy of Sciences 1431 Sofia. Bulgaria Abstract-

-The axonal transport of proteins to the nerve endings of Herbst and Grandry sensory receptors has been investigated by electron-microscope radioautography. Soon after the injection of [‘Hlleucinc into the trigeminal ganglia of young ducks. labeled proteins are conveyed along the suborbital sensory nerves to the sensory nerve endings at rates of at least 200-280 mm/day. Most of these rapidly transported proteins accumulate in areas containing vesicles of various kinds and along the axolemmal region. Later. the bulk of labeled proteins migrate along the axons at rates of about 15 mm/day and arc drstributed mainly to the mitochondria. A small portion of labeled material is transferred to the adjoining modified Schwann and specialized Grandry receptor cells. It is concluded that the transport of proteins from sensory ganglia to sensory nerve endings of mechanoreceptors IS conveyed at fast and intermediate rates and is mainly used for the renewal of vesicles. axolemmal constituents and mitochondris

The active transport of proteins from the neuronal cell body along the axon has been repeatedly demonstrated by labeling newly synthesized proteins with radioactive amino acids.2”.4”.54 Despite the similarities noted between the profiles of rapidly transported proteins in motor. sensory and sympathetic axons.s.7.5’ differences in the velocity and/or the amount of transported proteins exist even between the two branches of sensory neurons.32.34.4L.42~43.55 Although numerous studies have been devoted to axonal transport of proteins into parasympathetic nerve endings.‘.” vestibular epithelium.2 sensory axons and ganglia8-“.“‘.‘N.2”,3Y.53 no attention has been paid to transport into the sensory nerve endings. The large sensory nerve endings of avian mechanoreceptors featured by characteristic axoplasmic protrusions and an unusual accumulation of mitochondria and vesicles of various kindsi are advantageous in studying axonal transport into mechanoreceptors. Moreover. the large amount of axonally transported materials into the large sensory nerve endings. and the characteristic arrangement of modified Schwann cells and specialized Grandry receptor cells around them. provide an opportunity to study transfer of materials from the sensory ends of the neurons to the adjoining cells. The aim of the present study is to examine axonal transport of newly synthesized proteins and their destination in the nerve endings of Herbst and Grandry sensory corpuscles, which are very numerous in the hill skin of young ducks. EXPERIMENTAL Ten one-week-old

PROCEDURES

Peckin ducks weighing 40 + 1Og

were lightly anesthetized with chloroform and the right trigeminal ganglia were injected during IOmin with 250 pCi of r-[4,5-‘Hlleucine (specific activity 48 Ci:‘mmoi, Amersham International. England) dissolved in 10 ~1 of saline. Small samples of the skin of both sides of the upper bill were cut out at a distance of 25-30 mm from the ganglia at different time intervals ranging from 3 h to 14 days. The ganglia and suborbital nerves of some ducks were also excised. Material from the left side was used as a control. The samples were fixed in 4”,, paraformaldehyde freshly dissolved in 0.1 M phosphate buffer (pH 7.2), thoroughly washed in the same buffer and postfixed in 2”,, osmium tetroaide. They were then embedded in Durcupan ACM (Fluka) and processed for light- and electron-microscope radjoauto~r~lphy~3 using Word KS and L, nuclear emulsions. The light-microscope radioautographs were exposed i month at 4 C and developed in Kodak DlY. For electron-microscopy the specimens were exposed 2 months at 4~C and developed with phenidon.“’

Specimens made from each animal 6 h 1. 2. 7 and 14 days after injection were exposed and developed together and used for quantitativ,e analysis.‘h fifty-per-cent circles being used with a radius corresponding to 230 nm at a final magnification of 30.000. More than 800 silver grains were collected from each time interval. Because of the characteristic fine structure of sensory nerve endings. most of the silver grains and circles lay over the jtjnctional areas between cell organelles, the primary constituents being only mitochondriu and vesicles of various kinds. The microtubules occupied only a very small relative volume as did the vesicles. The cells adjoining the nerve endings (the modified Schwann cells and the specialized Grandry receptor cells) were divided into two zones: an inner zone I500nm WI& in direct contact with the nerve ending, and nn outer zone comprising the rest of the cell. The silver grains over these two zones were counted separately. The

observed and expected frequency distributions WCIC conpared with the chi-square test. The grain c‘uurIIs LVCIC finally transformed into grain density value\ /(:I r’;ici\ primary item.

RESULTS

General structure of Herbst and Grandry sensory corpuscles The Herbst corpuscle is an ellipsoidal body (300 x lOO@m) the central core of which is occupied by the centrally situated sensory amyelinated nerve fibre and its enlarged nerve ending, surrounded by symmetrically-arranged cytoplasmic processes of modified Schwann cells. An outer capsule is composed of concentrically-situated perineural cells reinforced by collagen fibres. The subcapsular space contains collagen bundles and single fibroblasts and macrophages (Fig. 1A). In the Grandry corpuscle (50 x 15 pm) two specialized receptor cells enclose the non-myelinated sensory nerve fibre and its large nerve ending (Fig. 1B). Their cytoplasm contains numerous dense-core vesicles (120-180 nm) (Fig. 2) and filaments. Modified Schwann cells surround the specialized cells, theil cytoplasmic processes abutting upon both poles of the sensory nerve ending. The capsule is similar to that of the Herbst corpuscle. The most important parts of both corpuscles are the large nerve endings (15-40 pm wide) and the Schwann and Grandry cells adjoining to them. The nerve endings are rich in mitochondria and vesicles of various kinds, clear ones predominating. The ax+ lemma forms characteristic processes’3 which contain only microfilaments and clear vesicles. The microtubules and the neurofilaments are conspicuous in the axoplasm of the preterminals. but they are rarely observed in the nerve endings. Light-microscope

The rcyult\ 0T slectron-mlcl-o~c,jpi. rj~ilroa~rl~~~~~l~t~!, .~rc III lint uith Iha~ of light-riiiLil,~ci,r)l~ dat,\. 1.1~ sensor> ncrst’ cndingh arc moth. ilC:irllj iabel& flJ,;i: any other str’ucturcs in both Herbs{ .~!rd (irantir! C‘OI.

pusclesdurmg the period from .I I; :.: i-4 da!\ ;tl’icr tlx injection radioacti\it,

(Frps

2. 3. 4) A

!5 alw

found

siniii;il oxi

tlw

i;wcc’nlra!w~

i: i

,l)l::i-;~rnleii,1‘~(.,li < 1‘ )r

prrterminal~. At all tune ~ntcr-v;A .riid&. ti;iL PI-Cterminals show higher activity ~hrir~ W+WWIIS !ti>catcd more proximally from the ncr\e cnd:i~~\ From 3 11 to I d3~. most of !iic hilici- grama ;trc located over areas containmg vesicles :md compound areas including vesicles. axolernma ;LH~adjoining cells (Figs 3 and 51. At these early time inlcrvals. the mitochondria account for on& a negllgiblc part r.s till the second day and after that diminishes progrossivcly. being always higher than that of the \zsiclc:, {Fig> 4 and il. The repior, of oynaptic‘II:J ~l~~sli-rosolnc-like densities do not show an) promine:li ;icliVitiei; Mompal-cd with other regions. A small number of silver grains ale i~a~ctl over the inner zone of the adjoining cells. R;rdioactivit> rises slightly until the second day and remains at an almost constant level with ;I slight tendenq 1r1 decrease. Radioactivity in the outer zone reack :t maximum at day I then diminishes rapidly being aiuaq’s less than that in the inner lone (Fig. 51. Only occasional silver grains arc iound ot’cr the myelin sheaths and the periphery 01‘ the receptors. as well as over connective tissue cells. b!ood vessels and perineum1 capsular cells.

radioautographJ

An intensive labeling over most of the ganglion cells is observed 15 min after the intraganglionic injection of C3H]leucine. Labeling over the suborbital nerve fibres which supply the receptors appears at a distance of 15 mm from the ganglia within 1~l/2 h after the injection. The intensity of the labeling is very low but increases several-fold within the l-7 day time intervals (Fig. 1C). The sensory nerve endings are the site of a strong radioautographic reaction between 3 h and 14 days after the administration of labeled leucine (Fig. 1A and B). Three hours after the injection only Single silver grains lie over the nerve endings, but their number increases steeply to reach a maximum by the first day. This strong reaction is maintained for 7 days, afterwards it gradually decreases. The adjoining cells are the site of weak but relatively constant labeling. It is more pronounced than in the capsule and the subcapsular space, or over the receptors of the contralateral side.

II IS well known lhal most (>I‘ the tadioactlvlr~. which remains iu the tissue> of animals qected with radioactively labeled amino acids and \ubsequenti) prepared for radioautograph). ib prssent in newI) 1-l ,hlr\ <,f ,hc synthesized proteins. ,.I-.19.?4.Jla injected [ ‘H]leuc~nc IcaL> Into th
_. _., Fig. 2. Heavy accumulation of silver grains over the sensory nerve ending of Grandry corpus$ 2 da)‘% after [3H]leucine administration. Grandry receptor cell (G). preterminal (arrow). 2. 13.tMt~

.

:

r’

At

1 day

after the C3H]leucine along

the axolemmal

administration region

most of the silver

of a Grandry

137

grains

nerve ending.

lie ov ‘er the I

x 30.000.

nd

Axonal

transport

of proteins

into sensory

nerve endings

-

Mitochondria

o-

-

-c

_ e-

I&

,

Vesicles inner zone

-

4

Outer

zone

of adjoining

cells

of adjoining

cells

xz

6

-B----_-_T_ ‘*---_‘_-------*

A/

6h

’

Id

I

2d

I

14d

7d Time

after

injection

Fig. 5. Time curves of the grain density over the sensory nerve endings and the adjoining after the intra-ganglionic injection of [3H]leucine.

ings, where only occasional silver grains were associated with the vesicles and mitochondria. These data, together with the gradual increase of labeling from the trigeminal ganglia L.I’LI the suborbital nerve fibres to sensory nerve endings, indicate that most of the label detected by radioautography does correspond to proteins synthesized in the neuronal cell bodies and transported somatofugally within the axons. The probable velocity of the fast moving fraction of these proteins is estimated to be at least 2OtL240 mmjday since it covers the distance of 25 mm to the receptors in less than 3 h. Although the data indicate that some of the radioactive proteins are rapidly transported. a much slower moving portion of the proteins is evidenced by the peak of radioactivity which appears between 1 and 3 days. Most of these proteins migrate along the axons at approximately 15 mm/day. Similar rate of 20 25 mm/day has been reported in the sensory part of the rabbit vagus nerve.2’.‘2 Moreover, the kinetic analysis of transported proteins into chohnergic neuron?.’ ’ Indicates that more than 95”,, of the slowly migrating proteins do not reach the nerve endings. Our results are in agreement with these observations. The most slowly moving portion of axonally-transported proteins (1 2 mm/day)34,“” is not detected in the mechanoreceptors. This may be due to the poorly developed cytoskeleton of sensory nerve endings which is conceivably supplied with the slowest wave of the axonal flow.36 The intermediate rate of protein transport may reflect the persisting growth of the suborbital nerve fibres in young ducks.

although

the development

receptor

of receptors

cells

at this stage is

already completed.“(’

The relative volume occupied by vesicles in the axoplasm of the sensory nerve endings shows a great diversity. Among the populations of clear and coated vesicles, single dense-core and double vesicles can also be identified. The functional role and the presumptive synaptic nature of vesicles in the sensory nerve endings is far more unclear and obscure than in the terminals in the central and peripheral nervous system. Until day I, the areas rich in vesicles contain more label than all other regions of sensory nerve endings. Thus, it can be assumed that most of the newly synthesized proteins rapidly transported to the sensory nerve endings are associated with the vesicles. It is now widely accepted that the axonally-transported proteins move as constituents of cytological structures.3”.3h as has been suggested for the synaptic vesicles in sympathetic”~22~2’~*8~z9~‘2 and parasympathetic ne~r0n~,l5.lh.3~.4S The fall in radioactivity after 1 day reflects a high turnover rate of some proteins, probably related to transmission of the afferent nerve impulses or a transfer to other cell organelles or both, The low resolution of the electron-microscope radioautography does no permit accurate estimate of the presence of radioactive material in the axolemma. An argument in favour of incorporation of newly synthesized proteins into the axolemma comes from the fact that the real grain counts over the compound

items.

including

are 40 70”,,

the axolemma.

higher

than those predicted

when the axolemma

itself is not

taken

It

that

into

proteins

account.

axonal

smooth

10 the ;ixolemmu

endoplasmic

It is well known along

has been shown

are transferred

mm,:day”’

but there is evidence

of these organelles.“~2”~J’

fast

slower

mitochondrial than

materials. endings expected wily.

that

of

more

radioactivity

in to

nerve

data

endings

transport

in the perykaria.

ported

to

declines. suggest

of the mitochondrial

sensory

axonal

be wl-

continues

vesicles

3. These

portion

can

transport

density the

at day

the

the

in the nerve than

axonal

In

a negligible

afforded

their grain

a maximum

of

can

be

mitochondria

This conclusion

IS also &up-

by the lack of a second peak of mitochondrial

radioactivity and

of

of

generally

rapidly-transported Iaboled

their

reaching only

other

radioactivity

after

the velocity being

the mitochondria

on the basis

Furthermore.

labeled

the

intensivclp

increase that

for both slow and fast

transport

In our study. are

arc transported

sciatic nerve at a rate of only a few

movement the

the

reticulum.“

that mitochondria

the chicken

glhw-

from

observed

resulting

port. “A’ tivity

from

in other the

The major

part

cndoplasmic

the outer

It

is

amount

conceivable of material

be incorporated release

membrane

endoplasmlc

The

that

is in contact

with

that

each

axon

releases

sonic

which

could

into its surroundings

by adjacent nature

of

~~11s.~~ Most in rhe region

this

material

and the predominance

knt)wtl.“‘.“.”

the nerve endthe finding

retictlluni.‘J.~“.“’

is more pronounced

endings.

tranbradioac-

the vesicles of the

within

IS in line with

mitochondrial

the smooth

from

reticulum

ings. This assumption

models

mitochondrial

of mitochondrial

seems to be transferred

smooth

cxperimcntal

slo\v

likely

this

of the ncrvc is

not

>ct

of polypeptide

RE:tEREN(‘f!S I. Austin

L.. Bra); J. J. 8.1 Young

,h’uurochtn~.

1. Alvarez

13, J. &

vestibular 3. Appletauer

I Zhi

R. J. (1966)

Transport

of proteins

and

rihonucleic

acid AWp

ncrjc‘ ,t\om

.I

1269.

Piischel

M. (1072)

system. Bruit

Transfer

of rnaterlal

from

cffercnt

aion<

ro sensor!

eplthcllum

in lhc goldti
RCY 37, 265 274

G. S. L. & Korr

1. M. (1077)

Further

stud~rson proteins ()I’ rlsurlWal ori’lns

electrophorctlc

11,hhLLIC1;11

muscle. E.syl. .Ve1o0/. 57, 713 7-34. 4. Barber

P. C.. Perry

specific transneuronal

I>. M..

Field

transport

P. M. & Raisman

G. (lY7X)

tlec[ron-mlcti)scopL

in the mouse accessory olfactory

J. L.. Neale J. H. & Gainer H. (1976) Rapidly transported of the isolated frog nervous system. Bruirl RYS. 105. 497 5 15.

5. Barker

6. BennettG., DiGiamberardino

L.. Koenig

H. L. & Dro7

B. (lY73)

* autoradlographlc

bulb. Rrcrin Krs. 152. 33

c\idcncc

proteins in sensory. motor and sqmpalhsttc Axonal

migrarion

f01

3011

of protelu

iicr\c’\

and gi~coprotc~n

111

II. Radioautoradiographic analysis of the renwal of glycoprotelns in nerve endings of chicken ciliarb nerve endings ganglion after intracerebral injection of [‘H] fucosc and [‘Hlglucosamine. Broirt RCS. 60. 12’) I46 7. Risby M. A. (1977) Similar polypeptide composition of fast transported proteins in rat motor .md ~nsor~ axons. .I ,Veurohiol. 8, 303. 314 8. &sby M. A. (1978) Fast axonal 281 -300.

transport

of labeled protem

tn sensory axons during

rcgeneratlon.

1:x/‘/. .~~*rtrt*~ 61.

Axonal 9. Bisby M. A. (1981) Reversal

transport

of proteins

of axonal

transport:

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transport

into sensory

similarity

of proteins

of i4C proteins

111

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in anterograde

at two rates in chicken

and retrograde

sciatic nerve. Brrtirt Rrs. 12,

23&233.

11. BungeM. B. (1973) Fine structure

of nerve fibers and growth

cones of isolated

sympathetic

neurons

in culture.

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15.

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transport

A. M. & Austin

of protein

transport

of horseradish

peroxidase

enhanced

L. (1972) The Row of rnltocholldri~t in two branches

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axon\.

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by

des

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of labeled

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in sensory

fibres of rabbit

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in

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(‘. N. Chouchho\.

113 43. Ochs S.. Erdman fibre branches

J.. Jersild

44. Ochs S.. Johnson intra-cord

45.

Jacobson

W. (I 980) Smooth

J., Schonbach

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endoplasmic

111nervous

tissue:

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D. L.

from c‘.

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toilowung

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and axonal

transport.

9 1n bird\

In

.I. .%e~rrc~ci~c,~:: 35. 16~2.5,

Ntr&~r~~fi

0,’ Sc~rr\t~~.: !‘hr\ir)ioqr

(eti.

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phase ot axoplasmlc

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pro!
an clectron-

141. 485 49X.

componenta.

uptake

and retrograde

mechanisms

between

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and speciticlly.

mitochondrial

of tetanu-.

toytn

by ncrvc

analysis

of proteins

./. Vwd~ioi.

IO,

aspects of the aronal

outer

Rrr,. .VL’III.OS(X 2. -III’; 504, membranes

and agranular

reticulum

J. Crll Sri. 46, 129. I47

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tcceptoi

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an the dc~r~~il rG,,)t and nerbe

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materials

and axoplasm~c

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H. (1978)

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rncorporation

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stud!.

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49. Schwartz

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of cutaneous

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and G

.I i\‘t,~m)~ /wm 14. 1 I 7 1 1 I

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Development

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M.) vol. 0, pp. 33X 317. Springer

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I)

rapidly

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53. Theiler

R. F. & McClure

W

0.

( 1978)

Rapld

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J.

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Ci. W.

( 19x1)

The rate of fast transport

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Prny.

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F. P. & White

S. R. (1977) Characterization

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afferents M.

A

(1969)

The

assessment

of protetns

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at diRerent

rates b) axopktrrnrc

tiow m the

8, 315 314. of electt-on-microscol,iz

autoradqraphs.

.+idl.

O/jr!‘.

Elrc~r.

Zli~rr~sf.

3.