Aluminum chloride stimulates NACl-dependent release of taurine and γ-aminobutyric acid in rat cortical astrocytes

Pqeurochem lnt Vol lS, No 1, pp 125-129, 1991 Printed m Great Britain All rights reserved

0197-0186/91 $3 00+000 Copynghl ,c 1991 Pergamon Press plc

ALUMINUM CHLORIDE STIMULATES NAC1-DEPENDENT RELEASE OF TAURINE AND 7-AMINOBUTYRIC ACID IN RAT CORTICAL ASTROCYTES JAN ALBRECHT* a n d MICHAEL D. NORENBERG Veteran Administration Me&cal Center, Department of Pathology, University of Mmml School of Me&cme--Jackson Memorial Hospital. Mmml, FI_ 33101, U S A ( Recett,ed 21 March 1990, accepted 6 June 1990)

Abstract--The release of preloaded radlolabeled taurme (TAU) and ),-amlnobutyrlc acid (GABA) from cultured rat cortical astrocytes was monitored 15 mln before and 30 mln after pulse treatment wRh alummum chloride, at 5 rain intervals A1CIa at concentrations ranging from 0 125 to 1 mM stimulated TAU release to 252 and 519%, respectively, m a relatively dose-dependent manner Release of GABA was not affected by 0 5 mM but was almost doubled by 1 mM AIC1 ~ The effects of AIC1 ~were greatly dlmlmshed or abolished when lsotonlc sucrose was substituted for NaCI m the superfuslon medm Interaction ofAl ~+ ions with membrane transporters of amino acids is suggested to account for their increased release Possible neurophys~ologlcal consequences of the acute effects of aluminum on the neuroactlve amino acid transport in astrocytes are &scussed

a l u m i n u m results in m a r k e d morphological and ultrastructural changes ( N o r e n b e r g et a l , 1989). It m a y thus be hypothesized that disturbances of astroghal n e u r o n a l xnteractlons participate in the p a t h o m e c h a n l s m of a l u m i n u m - r e l a t e d neurological disorders It has been previously observed t h a t astrocytes respond to a n u m b e r of extracellular stimuli including h y p e r a m m o n e m i a (Albrecht a n d Rafatowska, 1987), elevated potassium (Bowery et a l , 1979, PasantesMorales a n d Schousboe, 1989, P h l h b e r t et a l , 1988, 1989), hypoosmolarlty (Pasantes-Morales and Schousboe, 1988), excltotoxins ( L e h m a n n a n d H a n s s o n , 1988, Gallo et a l , 1989) a n d l o n o p h o r e s (Bowery et a l , 1979, Sarthy, 1983), with a p r o m p t e n h a n c e m e n t of the efflux o f newly t a k e n up n e u r o t r a n s m l t t e r or n e u r o m o d u l a t o r y a m i n o acids Such increased neurot r a n s m i t t e r release is postulated to elevate the extrasynapt~c c o n c e n t r a t i o n s o f neuroactwe c o m p u n d s m vn'o, a n d consequently affect neural transmission Therefore, m the present study we examined the effects of AICI~ o n the n e u r o t r a n s m l t t e r release m cultured * Author to whom all correspondence should be addressed astrocytes The release of the inhibitory neuroat Department of Neuropathology, Medical Research t r a n s m i t t e r - - 3 , - a m m o b u t y n c acid ( G A B A ) - - a n d the Centre, Pohsh Academy of Sciences, Dworkowa St 3, inhibitory n e u r o m o d u l a t o ~ t a u r m e ( T A U ) was in00-784 Warszawa, Poland vestigated Since astrocytlc a m i n o acid t r a n s p o r t has Abbre'clatlons TAU, taurlne, GABA, ?,-amlnobutync acid, been previously d e m o n s t r a t e d to be sodium- a n d / o r AOAA, ammooxyacetlc acLd 125

A l u m i n u m is a n e u r o t o x m t h a t has been l m p h c a t e d in the pathogenesxs o f several neurological disorders including &alysls e n c e p h a l o p a t h y , Alzhelmer's disease a n d the P a r k l n s o n - A L S - D e m e n t x a complex o f G u a m Systemic or m t r a c e r e b r a l a d m l m s t r a t i o n of a l u m i n u m salts to experimental a m m a l s induces a w~de spectrum o f changes t h a t are typical of neurodegenerative disorders m h u m a n s (for a recent review see S t u r m a n a n d Wlsniewskl, 1988) W h d e n e u r o n s a p p e a r to be the m a j o r target of a l u m i n u m in the CNS, evidence suggests t h a t alumin u m also affects astrocytes. Dialysis e n c e p h a l o p a t h y is a c c o m p a m e d by spongy d e g e n e r a t i o n o f cerebral cortex with m a r k e d alterations in astrocyt~c processes ( W m k c l m a n a n d Rlcanatl, 1986), a n d by accumulation of a l u m i n u m in astrocytes ( G o o d a n d Perk 1988) F u r t h e r m o r e , reJection o f a l u m i n a gel into the rat cerebral cortex induces widespread ghosis (Harris, 1975) Finally, studies xn this l a b o r a t o r y have s h o w n that long-term t r e a t m e n t o f cultured astrocytes with

[ 2(+

JAN ,<\1111141( H I dnd MI( II %11 D

"N()RI HIll 14~,

:Au

c h h ) r l d c - d c p e n d e n t (SLhousboc, 1981, W a l l i c ~ k l and M d r i i n . 1984, P h i h b e r i cl <#/, 1989). ~c ab, o o \ allllll0d the eff0ct o f ~odlum c h l o r i d e on the ic,,pon``c to A N ' l ,

10 O --O

•

control

Na

V - - V 0 125 mM v---~" 025ram

8

0--0

05ram

6

E\PERIMENT%I

P R O ( EI)IJRES

AI

/ &

|~[ll)( ill( (lt/lllt~

The ,>tudte~ `auto perle1 reed on neonatal +,tt LOrllcdl dMl ogro`an ,i~ prevlOtisl'v d e s c r i b e d in the prc``encc ol dbcAMP ((~legorlo,, ct u/ 1985) hnmulmhlstochemic,ll dlldL~ Sl`` indicated thai el the cell population Confluent cullures rallglng in age Irom I 5 It+ () ~eeks ~ e l e u.,,ed

~"-+-. &

~°~°~o~ Ld O9

2

Ldie``

~/,i

,

Ld Z O

i

10

+o -; O--O @--0

FC)

I

control 05ram

Ne

-<

[ H
Loading el Ihc cells "~,lth hldl,.ilabelcd anllilt) aLld'~ dnd the ,,ubscquenl relc,p;e tesls were C,llried out c````entl
!+Ct ol [+H]GABA Ispecllic actnltx 4t) ('l mmol Nm~ England Nuclear. L I S A ) oi I H(i o f l ' H ] F A t i (speclhc +icti',it} :;5 ( ' i ' l n m o l . AnlershanL tl S A ) lor 16 ran1 dl 17 ( i n d i o t a t l n g w a l e r b a t h i h c c u l t u r c ' , w , erelheu`a4``hed ~; limes lor 3 111111and 5 times for 5 nlln each `alth I 1111o f the llledlunl `allhout iddloacil~,C colnpound~, Rcle,i``c ``ample`` `acie Ihcn coIMaed at 5 nllil inter,~,lN I\u d total el 45 rain II c. tj collet.tlon p¢llt:,ds) The cells ,~ere pul``c-treated for 4 111111~ l i h dlll'ormg LoncentrallOn,, o f Ale1, d u r i n g the f o u r t h ~_ollectitm period ( Figs 1 and 2) ~lt the end el the etperlnlelll, the cells `acre ``olubihzed in I tnI o f I M N a O H (I h, t7 ( ) Aliquot', OI the collected m e d i u m a n d ol the N d O H extlact,, `aele then a n d l b / e d b} liquid ``cnltlllation c o u n t i n g

61 O

AI

.\

r-1

"% 0 40

do

+

@~lr/~+t

,~

gd- +

7 o ...... 70 + - N 0

riME ( rain +

I I g I I tlcct~ el dlllClClll Lt+llLLlltidlltql'~ ill aitinlUltln+ Lhh)i ido (m I A t Icle,i,,c l'ioln ieprcsent`` lnCdll`` I'IOlH ddhl obhut]od I11 the e\pgrllllel]ls described lit ] able I ++i111,,tdndald tit', Idhon not e\eeednl~t "q)(+~,

2 5 t1111¢`` gre
( tl]I ll/UllcHl~

ic``ponsc', a t t a i n e d at (I q d n d 1 l ) n l M

l'he lele e\truded during the ``l\ collection periods aflet ~1(.'1+ hcatmcnt 'acre suinmaled dnd 'acre expressed
,,ignlllc
/ t~ ~e/t'uw A I ( I, Mlinulated the iclc
o/to

o__, of°J

AICI, ~serc 1/ot

dlli'cr,cii,l 11o111 itl
,%,, prc'~lOu<,l) o b ' , c r \ c d ( Ktllpl

The" M l n l u L i I O l } (Table

I)

w i t h c e r e b r a l cortic
a n d ()ja, 1983 ) ``tipl21+l"tlMtlll Of dMrot_\ to`` v~ lth


d¢l]clOnl

Driller

111 ~+lllch

NaCl

v~
``llttltod l o t b v i~,otonlc ``tlCl o``c, incl ca~od bdkLt] I+OlOd``C

el TAI_ When cxpre',,,¢d ll dl 20 111111 d11,21 c.'3~``dtltH1 el t h e M l l l / / l l U k

Hot3,e'~el

ilK" 101o
Alummum-mduced amino actd release from astrocytes

Table 2 Effect of aluminum chloride in the presence or absence of N a C I m the superfuslon m e d m m on the release o f G A B A from astrocytes m primary culture

GABA + No

10-

control 0,5 mM ~ lOmM

0--0 (I,--0 8'

•", - -

Release AICI~ conc (mM)

6

O •

4

I

AI

LIJ U3

I--~"

/

~zx~zx---..~_

0 (control) 05

~8~e--~--8~--~o

I0 ~no NaCI 1 0 - - n o NaC1

2 LLI [2C

o tO < n," LL

no Total radloactlwt)

°o Control

Z~

ZR

<2 z

127

0 10 O--O

Z~--~

control 1.0 mM

-

14 0 6 + 0 60 (8) 17 3 4 + I 49 (5) 24 82 + 1 47 (9)* 12 97+_0 55 (3) 13 10+_064(4)

100 123 176 92 93

Results are m e a n + S E M /or the n u m b e r o f experiments shown m parentheses * P < 0 05 as compared to the respective control with or without NaCI (one-v, ay A N O V A followed b> D u n c a n ' s test for multiple comparisons)

No

8

6 AI

GABA release

I

4

A...---- - A

2

40

50

60

70

80

90

TIME ( m m )

Fig 2 Effectsofdtfferentconcentrattonsofalummumchlortde on GABA release from astrocytes m the presence ( + Na) or absence ( - Na) of sodmm chloride Ftgure tllustrates the e×penments described in Table 2 For other detatls see legend to Fig 1

the end o f the o b s e r v a t i o n period (Fig 1) In the absence o f NaC1 (Ftg l, lower panel), 0 5 m M AICI~ inmally produced a shght decrease of T A U release, followed after 15 mln by a gradual mcrease This late increase was paralleled by a gradual rise o f control release, r e n d e r m g the net effect o f A1CI~ stattsttcally mstgnlficant (cf. T a b l e 1)

Table I Effect o f a l u m i n u m chloride in the presence or absence o f sodium chloride m the superfuslon m e d i u m on T A U release from astrocytes m primary culture Release AICI, ~.on~. (mM) 0 (control) 0 125 0 25 05 I0 ° noNaCI I) 5 no N a C I

°o Total radloactlwt> 3 32+_0 18 (7) 8 30+_0 39 (5)* 16 65+_ 1 05 (6)* 15 38+_1 24(9)* 1725+282(4)* 15 5 0 + 1 13(4) 18 1 7 + 2 2 5 (5)

% Control 100 252 502 463 519 467 545

Results are m e a n ± S E M for the n u m b e r o f experiments shov, n in parentheses * P < 0 05 as c o m p a r e d to the respective control with or without N a C I (one-way A N O V A followed by D u n c a n ' s test for multiple comparisons)

A1CI~ at 0 5 m M did not stgnlficantly affect G A B A release, b u t a 76% sttmulatlon above control release was observed at 1 0 m M AICI3 (Table 2) The release rate was maximal 10 m m after a p p h c a t l o n o f A1CI~, a n d thereafter showed a tendency to decrease d u r m g the last 10 m m , but dtd not return to the control level (Ftg 2, upper panel) In the absence o f NaC1, 1 0 m M A1CI3 dtd not increase total G A B A release (Table 3) The release rate d e m o n s t r a t e d a tendency to decrease d u r i n g the 10 m m following A1CI ~ treatment, followed by a tendency to mcrease at the later stage (Fig 2, lower panel) DISCUSSION

Previous investigations o n the neurotransmlsstonrelated m e t a b o h c effects of a l u m i n u m on m a m m a h a n C N S have dealt wtth whole brain tissue ( J o h n s o n a n d Jope, 1986a, 1987, Hoffstetter et al, 1987, Pendlebury et al, 1988), b r a i n slices ( J o h n s o n et al, 1989), or wtth nerve ending fractions (synaptosomes) ( J o h n s o n a n d Jope, 1986b, K o e m g a n d Jope, 1987, L t p m a n et al, 1988, further references m S t u r m a n a n d Wlsmewskt, 1988) The present study ts, to o u r knowledge, the first to d e m o n s t r a t e an acute effect of a l u m i n u m on n e u r o t r a n s m t t t e r t r a n s p o r t tn astrocytes

Possible mechamsms o! AICI ~-mduced release of TA U and GABA The m o s t slgmficant o b s e r v a t i o n of the present study was that T A U release was stimulated by A1CI~ c o n c e n t r a t i o n s below 0.5 raM, a n d that the sttmulatton at 0.5 m M A1CI~ was N a C l - d e p e n d e n t (Table 1, Fig 1) In further studies, it will be o f i m p o r t a n c e to evaluate the roles of N a + a n d Cl separately, as b o t h the two tons have been ascribed a dtfferent role in

128

IxN &LBRE(ftI and Ml(u,,[l

T A U release under different c o n d m o n s T A U release driven by ion a n d / o r water Imbalance. ] e by' hypotonic (Pasantes-Morales and Schousboe, 1988) or

high potassium medm (Pasantes-Morales and Schousboe, 1988) or high potassium media (PasantesMorales and Schousboe, 1989. Martin el a/ 1990a). was shown to be chloride-dependent and may' consist m T A U cotransport with chloride ions Interestmgly. TALl release ehclted b,, actp, auon of the noradrenerglc, and to some degrec by othcr neurotransm]tter receptors, and mediated by c A M P

(Madellan el al, 1985, Sham el a/, 1986) appears to be chloride-dependent as well (Martin el a / . 1990b) It may be recalled m this context that aluminum salts administered m i z~'o lncre,tse c A M P levels m rat cerebral co]rex (Johnson and Jope 1986a. 1987). and \\ hen added to cerebral cortical slices at mlcromolar c o n c e n t r a h o n s they. potentiate agomst-stmmlated c A M P production (Johnson el a l . 19891 11 thus appears hkely that aluminum ions exert theu stnnulators effect by actp,'atmg a chloride-dependent T A U transporter Recently, a predominantly chloridedependent T A U and G A B A out-transport has been shown Io operate m retinal cells (Pasantes-Morales cl al 1988 D o m m g u e z cf a / . 1989) Hov, e\er. the role ol Na + ions cannot be excluded, as so&urn has been sho\,,n to be reqmred Ik)r p o t a s s m m - m d u c e d T A L Jelease from cerebellar astrocytes (Phlhbert ct a/ 1989) Of interest In this context may. be the ulcreased basal T A U release obscrved m the absence of sodium (Fig I. Table I) This p h e n o m e n o n , wlnch was also obscr,ced in cerebral slices (Korp] dnd Oja. 1983) and ccrcbeltar astroc~tes (Phlllbcrt c/ a[. 1988b), has been speculated to be due to conI\)rmatumal changes m the sodium-dependent T A U transporter, fa'~ormg the outward T A I l transport (Korp~ and Ola, 1983) W h e t h e r a l u m m u m interacts with thp; transporter remains to be investigated A,, was the case wflh T A U the dependence o f Al('l~-stlmulaled G A B A release on the presence of NaCI m the m e d m m appears to be compatible with the Na ' - ol C1 -dependence o f the G A B A transporters m \ arlous cell type', of the CNS (cf Key.nan and Kanner. 19X8)

fhe ski\\ return to control ol the aluminumreduced release o f both T A I l and G A B A l'ollowmg cessation o f thc stimulus (Figs 1 and 2) contrasts with d usually rapid return to control release o f ; a n o u s amino aud.s t\~llowlng pulse tlc,ttnlclll O1" aMrocytes \\]th dlfl'erent recepto]- or ion tral]spolq coupled qnnull, such as lugh K ' (Pasante,,-Molales and Schou~boe, 1989) hypotonlc media (PasantesMorales and Schousboe. 1988)o~ excitatory amino

D N()RINBLR(,

acids (Gallo cl a/ 1989) More detailed Mtldles oil the mechamsm ol aluminum actmn \\ill help to disclose the lacto~(s) responsible I'or the long duration of the release

[)O~,~I/)/Cphl Wo/Oql[~I/

~lqlllfl( dll~ t' O/ dhllllllllllll-lll,'hl(

cd

ic/ca~c o! F I ( ' a m / O I B I

To unde, stand the rele,,ancc ol a h m m m m - m d u c e d relea',c o f T A I l and G A B A obselxed m this Mud\ r e l a m e to alumulum encephalopathy it is nccessa~ 3 to cons]dcl thc d o w s Ikmnd to reduce release Global brain a l n m m u m concentrations in aluminum-related neurological dlsmders reach 0 25 mM (for a rex]ex~ and relerences see Koemg and Jope. 1987~ hi this connection. Ihe slgmhcance ol ( ; A B A Ielca~,c obscrxcd at 1 (I mM AICI appcars unccrtaut ()1 interest, ho~e,,er, is the stnnulatlon o1" T A I l release obsel,,cd at. ol belo,a (1 2"~ mM AI( 1, ( onccntratlnnS belm~ 0 25 mM haxc prexlousl3 been obscrxed Io reduce a numbel ol I'tmctlonal]\ meaningful blochenucal changes m the ( NS such ds c g potentiation o[ n o r a d r e n a h n e leceptol-Sllmtlldted acctlmulallon ,.'fl c A M P m coltlcal slices (Johnson cl a / , 1989) or spccfl]c reductwn o f the l'aM phase ol potass|um-dependent calcltll]l influx lnlo % n a p t o s o m c s (Kocmg and lope 1987) TAIr has been postulated to be the m~oot d M r o g h a - d c l Ivcd l]Cnl o n l o d u ] a l o l

( [Ol d l s c u s M o l ] st.'C

Maltul c/ a / . 1988) Ilence. the Io,a alumlntunll]duced TA 1 ' l clea,,e I i Ol]l dS[I-OC} les Iqld\ Sel \ c as d ncuromodulatory (neuroprotectl,,c "1 signal I 1o\\ cxcl releaw of TAI from astrocxtes has also been ascribed an osmoregulato[y tunct]on (PasantcsMorale', and Schousboe. 1988. 1989) T A I l rclca,,c Illd", t h u s icpresent d n OMllOFCgUlatoly leSpOllSe Io alun]mtn]l chloride and this \,~ould ser,.c to counterdct astloc,,t]c sxxelhng While the effects o f sho]l-lelm [ l e d t l ] l e n t \\111] d l U n l l l l t l l l l c h l o l l d c Oll the dMrocx, tlC cell x~OlUl/lC ICnldlll [o b e l n x e M l g d t e d ] O l l g - t ¢ l n l exposure 10 tOXic ( ] I n M ) concentrations OI tJ]l'~ con]jlotlnd \\,is obselYcd to CatlSC aMI-OC~tlc \dcuoJl/ a t l o n ( N o r c n b e r g c ! a / 1989)

I¢~lll)ltl¢'ehl¢ltl~lllx VVC Ill,IRk 1)1 Rogcl 1 otllTcnhlscl [~H xaluablc advice and clltl~_al l e,ldmg ol the manuscllpt dnd Idll Kcllc\ Io~ help v,lth computing the dala and de~,lgnnle the ligmes l-he'aork ,,'~assupported by the Veterans AdrmnIMIdllOI1 dlld ,111 NIH B]omedl~.dl Rcwdtch Suppolt (Jlanl from the [ [111%el Silk of NI I,II111 RI~FFRI N(~F ~,

Alhlecht I dnd Rald|o~',kd t I I9871| nhant.edpntd~mm Mlllltlkllcd '-dlTIIIIObtl|\rlt_ d~-ld ICIcd%C b}

d'qFO(-~|C'~

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129

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