Chemoattractant-mediated increases in cGMP induce changes in Dictyostelium myosin II heavy chain-specific protein kinase C activities.

Dembinsky, Adi; Rubin, Hila; Ravid, Shoshana

doi:10.1083/jcb.134.4.911

Cited by 30 publications

(46 citation statements)

References 45 publications

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“…In that regard, three myosin II kinases have been cloned from Dictyostelium. Among them, MHC-PKC, a myosin II heavy chain-specific protein kinase C, is not expressed in the vegetative phase; it is specifically expressed during the developmental stage and is implicated in the regulation of myosin II translocation in response to chemoattractant cAMP when the cells aggregate to form fruiting bodies (Ravid and Spudich, 1992;Dembinsky et al, 1996Dembinsky et al, , 1997. MHCK A (Futey et al, 1995) and MHCK B (Clancy et al, 1997) belong to a novel class of protein kinases and are unrelated to conventional eukaryotic protein kinases.…”

Section: Discussionmentioning

confidence: 99%

Novel Myosin Heavy Chain Kinase Involved in Disassembly of Myosin II Filaments and Efficient Cleavage in MitoticDictyosteliumCells

Nagasaki

Itoh

Yumura

et al. 2002

MBoC

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We have cloned a full-length cDNA encoding a novel myosin II heavy chain kinase (mhckC) from Dictyostelium. Like other members of the myosin heavy chain kinase family, the mhckC gene product, MHCK C, has a kinase domain in its N-terminal half and six WD repeats in the C-terminal half. GFP-MHCK C fusion protein localized to the cortex of interphase cells, to the cleavage furrow of mitotic cells, and to the posterior of migrating cells. These distributions of GFP-MHCK C always corresponded with that of myosin II filaments and were not observed in myosin II-null cells, where GFP-MHCK C was diffusely distributed in the cytoplasm. Thus, localization of MHCK C seems to be myosin II-dependent. Cells lacking the mhckC gene exhibited excessive aggregation of myosin II filaments in the cleavage furrows and in the posteriors of the daughter cells once cleavage was complete. The cleavage process of these cells took longer than that of wild-type cells. Taken together, these findings suggest MHCK C drives the disassembly of myosin II filaments for efficient cytokinesis and recycling of myosin II that occurs during cytokinesis. INTRODUCTIONDuring cytokinesis, cells are pinched into two parts by constriction of contractile rings. The contractile rings contain parallel filaments of actin and myosin II, a configuration suitable for constriction of the ring, in animal cells (Mabuchi and Okuno, 1977;Mabuchi, 1986;Glotzer, 1997;Robinson and Spudich, 2000) and in the amoeba cells of the cellular slime mold Dictyostelium discoideum (Yumura and Fukui, 1985;Fukui and Inoue, 1991). It is known that disassembly of the contractile ring components, including the myosin II filaments, accompanies the progression of cytokinesis, ultimately leading to fusion of the opposing plasma membranes and separation of the two daughter cells (Yumura et al., 1984). Little is known, however, about how disassembly of myosin II filaments is regulated during this process.D. discoideum is a powerful experimental system that enables functional analysis of various myosin II mutants in the absence of the wild-type form (De Lozanne and Spudich, 1987;Manstein et al., 1989;Uyeda and Yumura, 2000). Through the use of such myosin II mutants, for instance, the functional significance of the phosphorylation of the three threonine residues at positions 1823, 1833, and 2029 in the tail region of Dictyostelium myosin II was demonstrated: their phosphorylation state regulates the assembly and disassembly of myosin II filaments (Kuczmarski and Spudich, 1980;Egelhoff et al., 1991Egelhoff et al., , 1993. One mutant in which alanine residues were substituted for the three threonines (3XALA myosin) mimics the dephosphorylated state and accumulates excessively in the equatorial region of mitotic cells (Egelhoff et al., 1993). In contrast, 3XASP myosin, in which the threonine residues are substituted with aspartate residues, mimics the phosphorylated state, cannot form bipolar filaments, and shows markedly reduced accumulation in the cleavage furrows . More recently, systematic mut...

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Section: Discussionmentioning

confidence: 99%

Novel Myosin Heavy Chain Kinase Involved in Disassembly of Myosin II Filaments and Efficient Cleavage in MitoticDictyosteliumCells

Nagasaki

Itoh

Yumura

et al. 2002

MBoC

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“…Our results directly address the nature of this requirement for cGMP in RLC phosphorylation: MLCK-A is indirectly activated by cGMP. Recent results by Dembinsky et al (48) demonstrate that a myosin heavy chain kinase is also indirectly activated by cGMP. The apparent inhibitory nature of cGMP on myosin phosphorylation remains to be clarified.…”

Section: Discussionmentioning

confidence: 99%

MLCK-A, an unconventional myosin light chain kinase from Dictyostelium , is activated by a cGMP-dependent pathway

Silveira

Smith

Tan

et al. 1998

Proc. Natl. Acad. Sci. U.S.A.

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“…The control of chemotaxis is even more complex; it requires the coordinated regulation of the actin cytoskeleton, the function of myosin II, and the unconventional myosins IB and IC (Schleicher and Noegel, 1992;Peterson et al, 1995;Chen et al, 1996;Wessels et al, 1996;Uyeda and Titus, 1997;Zigmond et al, 1997). One of the second messengers required for chemotaxis is cyclic GMP (cGMP), which is thought to function, in part, through a cGMP-dependent protein kinase to activate myosin II kinase (Dembinsky et al, 1996;Van Haastert and Kuwayama, 1997). Guanylyl cyclase activity is very rapidly and transiently stimulated in response to chemoattractants and requires a MAPK pathway distinct from that containing the MAPK ERK2 (Van Haastert and Van Lookeren Campagne, 1984;Ma et al, 1997;Van Haastert and Kuwayama, 1997).…”

Section: Introductionmentioning

confidence: 99%

A Novel Ras-interacting Protein Required for Chemotaxis and Cyclic Adenosine Monophosphate Signal Relay inDictyostelium

Lee

Parent

Insall

et al. 1999

MBoC

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We have identified a novel Ras-interacting protein from Dictyostelium, RIP3, whose function is required for both chemotaxis and the synthesis and relay of the cyclic AMP (cAMP) chemoattractant signal. rip3 null cells are unable to aggregate and lack receptor activation of adenylyl cyclase but are able, in response to cAMP, to induce aggregation-stage, postaggregative, and cell-type-specific gene expression in suspension culture. In addition, rip3 null cells are unable to properly polarize in a cAMP gradient and chemotaxis is highly impaired. We demonstrate that cAMP stimulation of guanylyl cyclase, which is required for chemotaxis, is reduced ϳ60% in rip3 null cells. This reduced activation of guanylyl cyclase may account, in part, for the defect in chemotaxis. When cells are pulsed with cAMP for 5 h to mimic the endogenous cAMP oscillations that occur in wild-type strains, the cells will form aggregates, most of which, however, arrest at the mound stage. Unlike the response seen in wild-type strains, the rip3 null cell aggregates that form under these experimental conditions are very small, which is probably due to the rip3 null cell chemotaxis defect. Many of the phenotypes of the rip3 null cell, including the inability to activate adenylyl cyclase in response to cAMP and defects in chemotaxis, are very similar to those of strains carrying a disruption of the gene encoding the putative Ras exchange factor AleA. We demonstrate that aleA null cells also exhibit a defect in cAMP-mediated activation of guanylyl cyclase similar to that of rip3 null cells. A double-knockout mutant (rip3/aleA null cells) exhibits a further reduction in receptor activation of guanylyl cyclase, and these cells display almost no cell polarization or movement in cAMP gradients. As RIP3 preferentially interacts with an activated form of the Dictyostelium Ras protein RasG, which itself is important for cell movement, we propose that RIP3 and AleA are components of a Ras-regulated pathway involved in integrating chemotaxis and signal relay pathways that are essential for aggregation.

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Chemoattractant-mediated increases in cGMP induce changes in Dictyostelium myosin II heavy chain-specific protein kinase C activities.

Cited by 30 publications

References 45 publications

Novel Myosin Heavy Chain Kinase Involved in Disassembly of Myosin II Filaments and Efficient Cleavage in MitoticDictyosteliumCells

Novel Myosin Heavy Chain Kinase Involved in Disassembly of Myosin II Filaments and Efficient Cleavage in MitoticDictyosteliumCells

MLCK-A, an unconventional myosin light chain kinase from Dictyostelium , is activated by a cGMP-dependent pathway

A Novel Ras-interacting Protein Required for Chemotaxis and Cyclic Adenosine Monophosphate Signal Relay inDictyostelium

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