Activation of the prespore and spore cell pathway of Dictyostelium differentiation by cAMP-dependent protein kinase and evidence for its upstream regulation by ammonia.

Hopper, Neil A.; Harwood, Adrian J.; Bouzid, Sadok; Véron, Michel; Williams, Jeffrey

doi:10.1002/j.1460-2075.1993.tb05900.x

Cited by 121 publications

(94 citation statements)

References 72 publications

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“…However, folate can also stimulate adenylyl cyclase, which we have shown requires ERK2 activation. The physiological significance of folate-mediated ERK2 and adenylyl cyclase activity is probably not for the relay of cAMP but for the activation of cAMP-dependent protien kinase, which is required at multiple stages of the life cycle (41)(42)(43)(44)(45)(46)(47)(48)(49). Interestingly, a more primitive Dictyostelium species, D. minutum, exploits a folic acid-related compound as a chemoattractant in the aggregation stage, suggesting chemotaxis toward folic acid and other folate-mediated responses may be very ancient in this group of organisms (50).…”

Section: Discussionmentioning

confidence: 99%

Activation of the Mitogen-activated Protein Kinase ERK2 by the Chemoattractant Folic Acid in Dictyostelium

Maeda¹,

Firtel²

1997

Journal of Biological Chemistry

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In this study, we show that folic acid activates ERK2 in developmentally regulated manner and is required for ERK2 stimulation of adenylyl cyclase activity. Maximum levels of folate-stimulated ERK2 activity occur in cells from very early in development, prior to aggregation, and again at the tipped aggregate stages, corresponding to the stages in which folate receptors and the coupled G␣ subunit G␣4 are maximally expressed. During the activation by folic acid, ERK2 is phosphorylated on tyrosine residue(s) and contemporaneously shows a mobility shift on SDS-PAGE. Interestingly, this activation is not elicited in the absence of G␤ subunits, in contrast to the response to cAMP. This response also requires the G␣4 subunit known to be required for other folic acidmediated responses (Hadwiger, J., Lee, S., and Firtel, R. (1994) Proc. Natl. Acad. Sci. U. S. A. 91, 10566 -10570). Furthermore, we show that the activation of ERK2 by cAMP is independent of the G␣4 subunit, while the activation of ERK2 by folate is independent of G␣2. Taken together, these data indicate that there are at least two pathways of ERK2 activation, heterotrimeric G proteindependent and -independent pathways. MAP 1 kinase cascades are used by eukaryotes to couple extracellular signals to diverse intracellular regulatory pathways. The diversity of these pathways is great and includes growth factor responses in mammalian cells, cell-type differentiation in Drosophila and Caenorhabditis elegans, mating and growth responses in yeast, and stress-mediated responses in yeast and mammalian cells. These cascades are mediated by various classes of G protein-and tyrosine kinase-coupled receptors (5-13). In Dictyostelium, three presumably independent MAP kinase cascades play essential regulatory roles during both growth and multicellular development. The MAP kinase kinase (MEK) DdMEK1 is required for chemotaxis toward cAMP during aggregation; ddmek1 null cells form very small aggregates but continue to differentiate into normally proportioned, but very small, fruiting bodies (14). DdMEK1 is specifically required at the time of cAMP stimulation for the activation of guanylyl cyclase and the production of cGMP, the second messenger for chemotaxis in these cells. Two MAP kinases, ERK1 and ERK2, have been identified and their functions characterized. ERK1 is required for vegetative growth and is thought to play roles during multicellular development (15), while ERK2 is required for the activation of adenylyl cyclase by the chemoattractant cAMP during aggregation, prespore-specific gene expression, and morphogenesis (2, 16). erk2 null cells are aggregation-deficient due to the inability to activate adenylyl cyclase and relay the cAMP signal but show normal activation of guanylyl cyclase, which couples to chemotaxis (17). erk2 null cells expressing a temperature-sensitive ERK2 show abnormal morphogenesis during the multicellular stages, as well as the inability to induce prespore gene expression when shifted to a nonpermissive temperature. ERK2 activity is induce ϳ...

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Section: Discussionmentioning

confidence: 99%

Activation of the Mitogen-activated Protein Kinase ERK2 by the Chemoattractant Folic Acid in Dictyostelium

Maeda¹,

Firtel²

1997

Journal of Biological Chemistry

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“…In the 1990s, it became clear that, in addition to extracellular cAMP, intracellular cAMP acting on PKA was also required for prespore differentiation and was, furthermore, essential for spore and stalk maturation and for the control of spore germination (Harwood et al, 1992;Hopper et al, 1993;Van Es et al, 1996). For stalk and spore maturation, cAMP is produced by adenylate cyclase R (ACR), whereas cAMP for induction of prespore differentiation and control of spore germination is produced by adenylate cyclase G (ACG) Van Es et al, 1996;Alvarez-Curto et al, 2007).…”

Section: Camp Regulation Of Fruiting Body Formationmentioning

confidence: 99%

Evolutionary crossroads in developmental biology: Dictyostelium discoideum

Schaap

2011

Development

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SummaryDictyostelium discoideum belongs to a group of multicellular life forms that can also exist for long periods as single cells. This ability to shift between uni-and multicellularity makes the group ideal for studying the genetic changes that occurred at the crossroads between uni-and multicellular life. In this Primer, I discuss the mechanisms that control multicellular development in Dictyostelium discoideum and reconstruct how some of these mechanisms evolved from a stress response in the unicellular ancestor.Key words: Evolution of multicellularity, Social amoeba, Encystation, Sporulation, Dictyostelium IntroductionThe social amoebas, or Dictyostelia, are a group of organisms that become multicellular by aggregation and then proceed to build fruiting bodies that consist of stalk cells and spores (see Glossary, Box 1). This developmental cycle is a response to starvation, and involves both highly coordinated cell movement and a tightly controlled programme of cell differentiation. Social amoebas belong to the supergroup of Amoebozoa (see Glossary, Box 1), a sister group to the clade of Opisthokonts (see Glossary, Box 1), which contains the animals and fungi. All supergroups contain unicellular protist-like organisms (see Glossary, Box 1) and, in several groups, multicellular life forms have evolved independently (Minge et al., 2009).The Amoebozoa supergroup consists mainly of unicellular amoeba-like organisms that have a simple life cycle. The feeding amoeba or trophozoite turns into a dormant cyst when faced with food shortage, drought or other life-threatening circumstances (Cavalier-Smith et al., 2004). Several clades of Amoebozoa have given rise to protostelid-like organisms (see Glossary, Box 1), which form a very simple fruiting body (see Glossary, Box 1) that consists of a single spore that sits on a simple stalk made by the same cell (Shadwick et al., 2009). However, only the Dictyostelia are able to form multicellular fruiting bodies that contain up to a million cells (Fig. 1).There are ~120 known species of Dictyostelia and a molecular phylogeny has been constructed to reveal the order in which they evolved (Schaap et al., 2006). The phylogeny subdivides species into four major groups (Fig. 2), with the model social amoeba Dictyostelium discoideum belonging to the most recently diverged group 4. Many species in groups 1-3 can still encyst as single cells when conditions are unfavourable for aggregation. However, group 4 species have lost the ability to encyst. Strikingly, all group 4 species tested secrete cyclic adenosine monophosphate (cAMP) to act as a chemoattractant for aggregation. This is most unusual, because almost all other organisms only use cAMP inside the cell to transduce the effect of other secreted stimuli, such as hormones, mating factors and neurotransmitters. None of the species in groups 1-3 uses cAMP for aggregation; some use glorin, a modified dipeptide of glutamate and ornithine, whereas others use folic acid, pterin or other as yet unidentified chemoattractants (Schaap e...

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“…(15 mM p-nitrophenylphosphate, 10 mM P-glycerophosphate, 1 mM Na3VO4, 0.4 ,uM microcystin-LR, 40 ,ug of aprotinin per ml, 10 jig of leupeptin per ml, 1 mM phenylmethylsulfonyl fluoride, 5 mM 2-mercaptoethanol, 20 mM imidazole. Western blots of the fractions using the anti-ERK1 antibody show a strong band with the mobility of ERK1 present in the 50 to 150 and 150 to 250 mM eluates from expressing strains but not from wild-type cells (Fig.…”

Section: Multicellular Development In Dictyostelium Discoideum Ismentioning

confidence: 99%

Identification and functional analysis of a developmentally regulated extracellular signal-regulated kinase gene in Dictyostelium discoideum.

Gaskins¹,

Maeda²,

Firtel³

1994

Mol. Cell. Biol.

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We have cloned a developmentally regulated mitogen-activated protein kinase (extracellular signal-regulated kinase) from Dictyostelium discoideum designated ERK1. Using anti-pTyr antibodies, we show that ERKI is phosphorylated on tyrosine in vivo and that it will phosphorylate myelin basic protein. The (16,26). As the aggregate forms, extracellular signals produced within the organism induce cell type differentiation and regulate morphogenesis. These events lead to the production of a migrating slug followed by culmination and the generation of a mature fruiting body containing spores and stalk cells (49,50,80). Biochemical and molecular genetic analyses over the last few years have identified components required for various aspects of these processes and have led to a further understanding of the regulatory pathways controlling development. Genes encoding membrane receptors, coupled GP and Got subunits, the effectors adenylyl cyclase and phospholipase C, and the transcription factor GBF have been cloned and analyzed at a molecular level (12,17,32,65,72,81,82 the membrane to those in the nucleus is cAMP-dependent protein kinase (PKA). PKA has been shown to be essential for aggregation, cell-type-specific expression of the ecmB gene, the induction of prespore cell differentiation, and the induction of sporulation and spore cell-specific gene expression (1, 27, 35, 36, 40, 56-58, 76, 77 (8, 21-23, 61, 79, 84). In metazoans, both G protein-and tyrosine kinase-coupled receptors regulate growth responses, gene expression, and cellular differentiation via MAPK-containing pathways (2,7,11,51,60,64,83). MAPK family members have also been shown to directly phosphorylate transcription factors in mammalian cells, including Myc, Elk, and Jun proteins, leading to an increase in the rate of transcription (14,29,38,46,59,74,75).

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Activation of the prespore and spore cell pathway of Dictyostelium differentiation by cAMP-dependent protein kinase and evidence for its upstream regulation by ammonia.

Cited by 121 publications

References 72 publications

Activation of the Mitogen-activated Protein Kinase ERK2 by the Chemoattractant Folic Acid in Dictyostelium

Activation of the Mitogen-activated Protein Kinase ERK2 by the Chemoattractant Folic Acid in Dictyostelium

Evolutionary crossroads in developmental biology: Dictyostelium discoideum

Identification and functional analysis of a developmentally regulated extracellular signal-regulated kinase gene in Dictyostelium discoideum.

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