CHEMOTACTIC SIGNALS AND RESPONSES ARE COORDINATED BY AN OSCILLATORY CIRCUIT IN DICTYOSTELIUM
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1 CHEMOTACTIC SIGNALS AND RESPONSES ARE COORDINATED BY AN OSCILLATORY CIRCUIT IN DICTYOSTELIUM Dr. William Loomis, UCSD (KITP Bio Networks Chemotaxis Workshop 3/12/03) 1
2 Dictyostelium is a social amoeba that separated from plants and animals about 1 billion years ago. Many genes and pathways are well conserved. animals Dicty plants Time ADVANTAGES The 34 Mb genome is sequenced. There are many well defined mutant strains. It grows well and billions of cells can be induced to develop synchronously. After 4 hours of development cells signal each other with and respond. Dynamics of spiral waves seen by dark-field microscopy; the cells contract when a wave passes over them but there is no net cellular movement Dr. William Loomis, UCSD (KITP Bio Networks Chemotaxis Workshop 3/12/03) 2
3 OSCILLATIONS IN LIGHT SCATTERING AND ADENYLYL CYCLASE Roos, W., Scheidegger, C., and Gerisch, G. (1977). Nature 266, RELAY GTP Ga2 car1 Gbg CRAC ACA Dr. William Loomis, UCSD (KITP Bio Networks Chemotaxis Workshop 3/12/03) 3
4 SIGNALING CIRCUIT Relay GTP car1 Ga2 Gbg CRAC ACA AMP ERK2 RegA R R C PKA (inactive) PKA C e pulse AGGREGATION STAGE NETWORK 5'AMP PDE CAR1 ACA i ERK2 REG A PKA Dr. William Loomis, UCSD (KITP Bio Networks Chemotaxis Workshop 3/12/03) 4
![INTERACTIVE NONLINEAR DIFFERENTIAL EQUATIONS WITH ACTIVATING AND DEACTIVATING TERMS [ACA]' = k1[car1]-k2[aca][pka] [PKA]' = k3[i]-k4[pka] [ERK2]' = k5[car1]-k6[pka][erk2] [RegA]' = k7-k8[erk2][rega]](/docs-images/93/117943240/images/5-0.jpg "[i]' = k9[aca]-k10[rega][i] [e]' = k11[aca]-k12[e] [CAR1]' = k13[e]-k14[car1] = differentiation with respect to time CIRCUIT OSCILLATES WITH A ROBUST 7 MINUTE PERIOD Dr.")
5 INTERACTIVE NONLINEAR DIFFERENTIAL EQUATIONS WITH ACTIVATING AND DEACTIVATING TERMS [ACA]' = k1[car1]-k2[aca][pka] [PKA]' = k3[i]-k4[pka] [ERK2]' = k5[car1]-k6[pka][erk2] [RegA]' = k7-k8[erk2][rega] [i]' = k9[aca]-k10[rega][i] [e]' = k11[aca]-k12[e] [CAR1]' = k13[e]-k14[car1] = differentiation with respect to time CIRCUIT OSCILLATES WITH A ROBUST 7 MINUTE PERIOD Dr. William Loomis, UCSD (KITP Bio Networks Chemotaxis Workshop 3/12/03) 5
6 PHASE SHIFT Phase shift Delay Advance Time of addition of pulse during 7 minute period ENTRAINMENT units minutes Dr. William Loomis, UCSD (KITP Bio Networks Chemotaxis Workshop 3/12/03) 6
7 APPEARANCE OF OSCILLATIONS DURING DEVELOPMENT Gerisch, G., Malchow, D., Roos, W., and Wick, U. (1979). J Exp Biol 81, e pulse AGGREGATION STAGE NETWORK 5'AMP PDE CAR1 ACA i ERK2 REG A PKA Dr. William Loomis, UCSD (KITP Bio Networks Chemotaxis Workshop 3/12/03) 7
8 OSCILLATIONS DURING EARLY DEVELOPMENT CHEMOTACTIC PROPERTIES OF VARIOUS STRAINS Mutant Signaling Directional Sensing Lateral pseudopods AX4 (none) periodic excellent few CAR1 none none --- ACA none poor --- ERK2 none poor many REGA poor poor many PKA-R poor poor many pulse AGGREGATION STAGE NETWORK 5'AMP PDE CAR1 ACA ERK2 REG A PKA Dr. William Loomis, UCSD (KITP Bio Networks Chemotaxis Workshop 3/12/03) 8
9 CHEMOTACTIC MIGRATION OF CELLS IN PURE POPULATIONS OF WILD TYPE (AX4) AND MUTANT (rega-) STRAINS CELLS LACKING RegA NEITHER SIGNAL NOR RESPOND Dr. William Loomis, UCSD (KITP Bio Networks Chemotaxis Workshop 3/12/03) 9
10 CELLS LACKING RegA MAKE MORE LATERAL PSEUDOPODS MYOSIN IS NOT RECRUITED TO THE CORTEX OF CELLS LACKING RegA Dr. William Loomis, UCSD (KITP Bio Networks Chemotaxis Workshop 3/12/03) 10
11 CHEMOTACTIC MIGRATION OF WILD TYPE AND PKA R- CELLS IN A PREDOMINANTLY WILD TYPE POPULATION CELLS LACKING PKA MAKE MORE LATERAL PSEUDOPODS Dr. William Loomis, UCSD (KITP Bio Networks Chemotaxis Workshop 3/12/03) 11
12 position of source * single anterior pseudopod in the front of a wave 3D RECONSTRUCTION OF A WILD TYPE CELL IN A CHEMOTACTIC WAVE new projections shown in red anterior pseudopod retracted at peak of a wave multiple pseudopods in the back of a wave In the front of a wave a cell experiences a spatial as well as a temporal gradient. Direction is established. Aggregation center direction of movement (slow relative to wave) Dr. William Loomis, UCSD (KITP Bio Networks Chemotaxis Workshop 3/12/03) 12
13 Distal cells are stimulated to secrete At the peak of the wave, the cortical layer of actin/myosin is dismantled and net movement ceases. In the back of the wave, the spatial gradient is reversed. The cell does not backtrack due to loss of cortical rigor and the formation of lateral pseudopods. Dr. William Loomis, UCSD (KITP Bio Networks Chemotaxis Workshop 3/12/03) 13
14 MODEL OF THE CHEMOTACTIC STAGES cgmp mediated basolateral inhibition of PI3K threshold (1 sec.) basolateral myosin II-based cortical rigor front of a wave (3 min.) a cell a cell recruitment of PH domain proteins; CRAC, PhdA etc. actin assembly; pseudopod formation movement loss of cortical rigor; lateral pseudopod formation back of a wave (3 min.) a cell no further net movement SIGNALING AND MOTILITY CIRCUIT Relay GTP Ga2 car1 Gbg CRAC ACA AMP ERK2 RegA R R C PKA (inactive) PKA C CONTROL OF CORTICAL RIGOR (directionality) Dr. William Loomis, UCSD (KITP Bio Networks Chemotaxis Workshop 3/12/03) 14
15 Dr. William Loomis, UCSD (KITP Bio Networks Chemotaxis Workshop 3/12/03) 15
16 Collaborators UCSD Michael Laub Sam Payne Wouter-Jan Rappel Gad Shaulsky Adam Kuspa Mineko Maeda Rick Firtel University of Iowa David Soll Deb Wessels The Albert Einstein Jeff Segall DYNAMICS OF CELLULAR RESPONSES TO A NATURAL WAVE Dr. William Loomis, UCSD (KITP Bio Networks Chemotaxis Workshop 3/12/03) 16
17 A human neutrophil chasing a bacterium ( S. aureus ) A time-lapse movie made by Dr. David Rogers at Vanderbilt in the 1950 s Dr. William Loomis, UCSD (KITP Bio Networks Chemotaxis Workshop 3/12/03) 17
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