Cycl i c 3' , 5' -AMP Rel ay i n
Di ct yost el i um di scoi deum
V. Adapt at i on of t he CAMP
Si gnal i ng Response
dur i ng c AMP St i mul at i on
ABSTRACT In Di ct yost el i um di scoi deum, ext r acel l ul ar c AMP act i vat es adenyl at e cycl ase, whi ch
l eads to an i ncr ease in i nt r acel l ul ar CAMP and t he r at e of c AMP secr et i on . The si gnal i ng
r esponse to a const ant CAMP st i mul us is t er m i nat ed af t er sever al m i nut es by an adapt at i on
mechani sm . The t i me- cour se of adapt at i on to st i mul i of 10-6 or 10 -7 MCAMP was assessed .
We used a per f usi on t echni que to del i ver def i ned c AMP st i mul i to [ 3 H] adenosi ne- l abel ed
amoebae and moni t ored t hei r secr et i on of [ 3 H] c AMP. Amoebae wer e pr et r eat ed with 10 -6 or
10 -7 M c AMP f or per i ods of 0 . 33- 12 m i nut es, and t hen i mmedi at el y gi ven t est st i mul i of 10 -8
Mto 2 .5 X 10 -7 Mc AMP. The r esponse to a gi ven t est st i mul us was pr ogr essi vel y at t enuat ed
and f i nal l y ext i ngui shed as t he dur at i on of t he pr et r eat ment st i mul us i ncr eased . Dur i ng
pr et r eat ment with 10 - 6 MCAMP, t he r at es of at t enuat i on coul d be r anked accor di ng to t he
concent r at i on of t he t est st i mul us . The r esponses to t est st i mul i of 10 - 8 , 5 X 10 - 8 , 10 -7 , or 2 .5
X 10 -7 Mc AMP wer e ext i ngui shed af t er - 1, 2 . 25, 2 . 5, and 10 m i n, r espect i vel y . 1 .5 m in of
st i mul at i on with 10 -7 MCAMP was necessar y to ext i ngui sh t he r esponse of a t est st i mul us of
10 - 8 M c AMP. Our dat a suggest t hat adapt at i on begi ns wi t hi n 20 s of st i mul at i on, r i ses r api dl y
f or -2 .5 m i n, and r eaches a pl at eau af t er - 10 m in . The absol ut e r at e of rise was f ast er dur i ng
pr et r eat ment with 10 - e t han wi t h 10 -7 M CAMP. These r esul t s suppor t a wor ki ng hypot hesi s in
whi ch t he occupancy of sur f ace c AMP r ecept or s l eads to changes in t wo opposi ng cel l ul ar
pr ocesses, exci t at i on and adapt at i on, t hat cont r ol t he act i vi t y of D . di scoi deum adenyl at e
cycl ase .
The aggr egat i on of Di ct yost el i um di scoi deum is medi at ed by
pr opagat ed si gnal s of cycl i c adenosi ne 3' , 5' -monophosphat e
( cAMP) . The si gnal i ng r esponse has been st udi ed bi ochem i-
cal l y ( 5, 13, 14) . The bi ndi ng of c AMP to cel l sur f ace r ecept or s
( 7, 8) l eads to t he act i vat i on of adenyl at e cycl ase ( 5, 12) , an
i ncr ease in t he l evel of i nt r acel l ul ar CAMP, and secr et i on of
t he newl y- synt hesi zed c AMP ( 5) . If t he st i mul us is wi t hdrawn
dur i ng t he r esponse, si gnal i ng prompt l y subsi des . Si gnal i ng
r esponses al so t er m i nat e spont aneousl y af t er a f ew m i nut es of
sust ai ned
st i mul at i on
as a r esul t of an adapt at i on pr ocess
( 3) .
The mechani sm of adapt at i on appear s to i nvol ve a r ever si bl e,
t i me-dependent decr ease in sensi t i vi t y to c AMP st i mul i . Ser i al
i ncrement s in t he l evel of ext r acel l ul ar c AMP evoke successi ve
si gnal i ng r esponses f ol l owed by adapt at i on to each new stim-
ul us concent r at i on . Duri ng aggr egat i on, adapt at i on pr esum-
abl y r egul at es t he magni t ude and dur at i on of c AMP si gnal i ng
554
MARY C . DI NAUER, THEODORE L .
STECK, and PETER N. DEVREOTES
Depart ment s of Bi ochem i st r y and Medi ci ne, The
Uni ver si t y of Chi cago, Chi cago, I l l i noi s 60637
r esponses and pr event s amoebae f r om r espondi ng per pet ual l y
to t hei r own secr et i ons .
We have pr evi ousl y shown t hat adapt at i on begi ns
to
i ncr ease
bef or e t he si gnal i ng r esponse t er m i nat es, per si st s
af t er t he
decl i ne of t he r esponse, and decays with f i r s t - or der ki net i cs
as
soon as t he CAMP st i mul us is r emoved ( 3, 6) . In
t hi s
i nvest i -
gat i on, we sought to def i ne t he t i me- cour se f or t he rise in
adapt at i on upon t he i nt r oduct i on of a c AMP st i mul us . As a
wor ki ng hypot hesi s, we assumed t hat a st i mul us, per cei ved as
an
i ncr ease
in t he
f r act i onal occupancy of cel l sur f ace
c AMP
r ecept or s, pr oduces changes in bot h an exci t at i on pr ocess t hat
l eads to act i vat i on of adenyl at e cycl ase, and an opposi ng
pr ocess, adapt at i on, t hat bl ocks such act i vat i on ( 6) .
If t hi s hypot hesi s is val i d, t he l evel of adapt at i on m i ght be
det ect ed at any time dur i ng t he si gnal i ng r esponse by i nt er -
r upt i ng t he st i mul us and subst i t ut i ng a t est st i mul us of l ower
Ti t s J OURNAL OF CELL BI OLOGYzyxwvutsrqponmlkjihgfedcbaZYXWV " Vot ut i +E 86 AUGUST 1980 554- 561
©The Rockef el l er Uni ver si t y Pr ess - 0021- 9525/ 80/ 08/ 0554/ 08 $1 . 00
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Published August 1, 1980