A non-canonical Grb2–PLC-γ1–Sos cascade triggered by lipovitellin 1, an apolipoprotein B homologue

Browaeys-Poly, Edith; Broutin, Isabelle; Antoine, Anne-Frédérique; Marin, Matthieu; Lescuyer, Arlette; Vilain, Jean‐Pierre; Ducruix, A.; Cailliau, Kátia

doi:10.1016/j.cellsig.2007.08.002

Cited by 7 publications

(10 citation statements)

References 51 publications

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“…The fact that the siRNA-mediated knockdown of PLC␥1 and PLC␥2 abolished the interaction between plexin-B1 and Grb2 indicates, however, that Grb2 is brought to the plexin-B receptor complex through its interaction with PLC␥ rather than through the direct interaction with the phosphorylated receptor. Grb2 could interact with PLC␥ directly through an interaction of its SH3 domain with a proline-rich domain of PLC␥, as recently described (6). Alternatively, it is conceivable that Grb2 and PLC␥ interact indirectly through a protein able to interact with both Grb2 and PLC␥ like LAT (8).…”

Section: Discussionmentioning

confidence: 93%

Semaphorin 4D Signaling Requires the Recruitment of Phospholipase Cγ into the Plexin-B1 Receptor Complex

Swiercz

Worzfeld

Offermanns

2009

Molecular and Cellular Biology

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The semaphorin 4D (Sema4D) receptor plexin-B1 constitutively interacts with particular Rho guanine nucleotide exchange factors (RhoGEFs) and thereby mediates Sema4D-induced RhoA activation, a process which involves the tyrosine phosphorylation of plexin-B1 by ErbB-2. It is, however, unknown how plexin-B1 phosphorylation regulates RhoGEF activity. We show here that activation of plexin-B1 by Sema4D and its subsequent tyrosine phosphorylation creates docking sites for the SH2 domains of phospholipase C␥ (PLC␥). PLC␥ is thereby recruited into the plexin-B1 receptor complex and via its SH3 domain activates the Rho guanine nucleotide exchange factor PDZ-RhoGEF. PLC␥-dependent RhoGEF activation is independent of its lipase activity. The recruitment of PLC␥ has no effect on the R-Ras GTPase-activating protein activity of plexin-B1 but is required for Sema4D-induced axonal growth cone collapse as well as for the promigratory effects of Sema4D on cancer cells. These data demonstrate a novel nonenzymatic function of PLC␥ as an important mechanism of plexin-mediated signaling which links tyrosine phosphorylation of plexin-B1 to the regulation of a RhoGEF protein and downstream cellular processes.Mammalian semaphorins were originally identified as axon guidance factors but are now recognized also as important regulators of morphogenesis and homeostasis in various organ systems, including the immune, cardiovascular, and renal systems (3-5, 7, 19, 23, 30, 35, 40, 56, 64, 76). Most effects of semaphorins are mediated by a group of large transmembrane proteins called plexins, of which four families exist in the mammalian system: plexin-A1 to -4, plexin-B1 to -3, plexin-C1, and plexin-D1 (60, 61). The four members of the plexin-A family in most cases require neuropilins as ligand binding partners to respond to semaphorins, whereas the three members of the plexin-B family are directly activated by semaphorins. While plexin-B1 binds Sema4D, plexin-B2 can be activated by Sema4C and Sema4D, and plexin-B3 has been shown to respond to Sema5A (31,35).The activation of plexins by semaphorins initiates a variety of signaling processes, which involve several small GTPases of the Ras and Rho families (31,34,43). All plexin family members possess an R-Ras GTPase-activating protein (GAP) domain (36). Activated plexin-B1 and -A1 have been shown to also interact with other small GTPases, including GTP-bound Rac1 and RhoD as well as Rnd1, Rnd2, and Rnd3 (14,37,48,63,67,68,74). Different from other plexin families, the C terminus of B-family plexins contains a PDZ domain-binding motif which mediates a stable interaction with the guanine nucleotide exchange factors PDZ-RhoGEF and LARG (1,15,26,39,57). Activation of the plexin-B1/PDZ-RhoGEF complex by semaphorin 4D (Sema4D) results in RhoA activation downstream of plexin-B1 (15, 39, 57). Members of the plexin-B family also interact with and are phosphorylated by the receptor tyrosine kinases ErbB-2 and c-Met (12, 22, 58). ErbB-2-mediated phosphorylation of plexin-B1 is required for plexinmediated ...

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Section: Discussionmentioning

confidence: 93%

Semaphorin 4D Signaling Requires the Recruitment of Phospholipase Cγ into the Plexin-B1 Receptor Complex

Swiercz

Worzfeld

Offermanns

2009

Molecular and Cellular Biology

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“…Because of its distinct subcellular distribution, it has been suggested that pp25 plays different roles than those of yolk-associated proteins. Browaeys-Poly et al (2007) reported that LV1, a larger fragment of vitellogenins, is partly cytoplasmic in Xenopus oocytes and that the cytoplasmic LV1 is phosphorylated at tyrosine residues and can serve as a scaffold for a signaling complex containing the adaptor protein Grb2, the guanine nucleotide exchanging factor Sos, and the phospholipase Cγ. The present study demonstrated that LV1 solubilized from the yolk materials of Xenopus oocytes can be effectively phosphorylated by purified Src.…”

Section: Discussionmentioning

confidence: 99%

Characterization of Lipovitellin 2 as a Tyrosine-Phosphorylated Protein in Oocytes, Eggs and Early Embryos ofXenopus laevis

Kushima¹,

Mammadova²,

Hasan³

et al. 2011

Zoological Science

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A tyrosine-phosphorylated protein of 33 kDa is shown to be present in the solubilized yolk fraction of Xenopus laevis oocytes, eggs, and early embryos. The phosphoprotein is lipovitellin 2 as demonstrated by immunoprecipitation and mass spectrometry studies, and is termed pp33/LV2. Sub-cellular fractionation and immunoblotting studies demonstrate that pp33/LV2 is stably present in the Triton X-100-resistant and SDS-soluble yolk fractions during oogenesis, oocyte maturation, and early embryogenesis. From after the swimming tadpole stages (stage 39∼), however, it becomes partly soluble to Triton X-100-containing buffer and all disappear thereafter (stage 48∼49). In vitro enzyme assays with the use of the tyrosine phosphatase LAR and the tyrosine kinase Src demonstrate the reversible nature of the tyrosine phosphorylation of pp33/LV2. Microinjection studies demonstrate that the solubilized yolk fractions, but not those immunodepleted of pp33/LV2 or those pretreated with LAR, inhibit progesterone- or insulin-induced oocyte maturation. A pp33/LV2-like protein seems to present in two Xenopus subspecies, one other frog species, and two fish species, but not in other amphibian species, such as newt and salamander. These results suggest that LV2, in its tyrosine-phosphorylated form, serves in a cellular function in a species-specific manner, but the mechanism is still unknown.

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“…In particular, tyrosine phosphorylation of LV2 is unusually stable during oogenesis, oocyte maturation, and early embryogenesis until the removal of yolk-associated materials from swimming tadpole (Kushima et al 2011). Possible function of tyrosine-phosphorylated form of Xenopus LV1 and LV2 so far suggested is oocyte maturation (Browaeys-Poly et al 2007;Kushima et al 2011), although it's upstream (liver or oocyte) kinase and downstream cellular function is uncertain.…”

Section: Lipovitellin (Lv)mentioning

confidence: 99%

“…It is well known that phosvitin and pp25 are highly serine/threoninephosphorylated proteins that serve as an energy source of oogenesis and early embryogenesis. On the other hand, tyrosine phosphorylation of LV1 (Browaeys-Poly et al 2007) and LV2 (Kushima et al 2011) has recently been demonstrated in Xenopus. In particular, tyrosine phosphorylation of LV2 is unusually stable during oogenesis, oocyte maturation, and early embryogenesis until the removal of yolk-associated materials from swimming tadpole (Kushima et al 2011).…”

Section: Lipovitellin (Lv)mentioning

confidence: 99%

“…In Xenopus oocytes expressing fibroblast growth factor receptor/kinase (FGFR), some Grb family members (Grb7, Grb10, and Grb14) have been implicated in tyrosine kinase-dependent signal transduction (Cailliau et al 2003). Microinjection of Grb2 into immature Xenopus oocytes has been shown to cause oocyte maturation in a Ras-dependent manner (Browaeys-Poly et al 2007;Cailliau et al 2001). In this unusual, but interesting oocyte maturation system, SH2 domains and SH3 domain of Grb2 interact with tyrosine-phosphorylated lipovitellin 1 and PLC, respectively.…”

Section: Grb2/7/10/14mentioning

confidence: 99%

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Phospho-Signaling at Oocyte Maturation and Fertilization: Set Up for Embryogenesis and Beyond Part II. Kinase Regulators and Substrates

Hasan¹,

Mutoh²,

Kihira³

et al. 2012

Embryogenesis

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A non-canonical Grb2–PLC-γ1–Sos cascade triggered by lipovitellin 1, an apolipoprotein B homologue

Cited by 7 publications

References 51 publications

Semaphorin 4D Signaling Requires the Recruitment of Phospholipase Cγ into the Plexin-B1 Receptor Complex

Semaphorin 4D Signaling Requires the Recruitment of Phospholipase Cγ into the Plexin-B1 Receptor Complex

Characterization of Lipovitellin 2 as a Tyrosine-Phosphorylated Protein in Oocytes, Eggs and Early Embryos ofXenopus laevis

Phospho-Signaling at Oocyte Maturation and Fertilization: Set Up for Embryogenesis and Beyond Part II. Kinase Regulators and Substrates

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