Concentration- and time-dependence of phosphorylation events stimulated by fibroblast growth factor-4 (FGF-4) in Rama 27 fibroblasts

Gradients of FGFs are an essential feature of many developmental processes. Thus, FGF2 stimulates different responses at high and low concentrations, while FGF4 gradients are critical, e.g., in limb development., but it is not known if responses to FGF4 differ in a concentration-dependent manner. Em...

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Hauptverfasser: Alsadun, Marim M., Su, Dunhao, Yates, Edwin A., Fernig, David G.
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Sprache:Englisch
Veröffentlicht: Cold Spring Harbor Laboratory 11.05.2025
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Abstract Gradients of FGFs are an essential feature of many developmental processes. Thus, FGF2 stimulates different responses at high and low concentrations, while FGF4 gradients are critical, e.g., in limb development., but it is not known if responses to FGF4 differ in a concentration-dependent manner. Employing rat mammary (Rama) 27 fibroblasts, we therefore measured the FGF4 concentration- and time-dependence of the simulation of phosphorylation of FRS2α, MAPK1 and MAPK3 which are downstream of the FGF receptor (FGFR1c). At 10 pg/mL FGF4 caused a very weak phosphorylation of FRS2α at Y435 and Y196 and a stronger one of MAPK1 and MAPK3 that oscillated with maximum levels after 30 min and 240 min stimulation. The phosphorylation of these proteins at 1 ng/mL FGF4 was considerably stronger and showed a similar oscillation. At 10 ng/mL FGF4, the phosphorylation of FRS2α reached an early peak after 5 min, declined at 15 min and then rose again at 30 min before declining to the end of the time-course at 240 min, whereas the phosphorylation of MAPK1 and MAPK3 was strong after 5 minutes, reached a maximum after 30 minutes and then declined gradually. At 1 µg/mL and 3 µg/mL FGF4 after 15 min and 60 min the phosphorylation of FRS2α, MAPK1 and MAPK3 was much lower at 60 min compared to that observed at lower concentrations of FGF4. The data indicate that at low concentrations FGF4 elicits an oscillatory response at the level of phosphorylation of FRS2α and of MAPK1 and MAPK3, whereas a bell-shaped dose response may occur at the highest concentrations of FGF4. The addition of exogenous heparin, an effective mimic of endogenous heparan sulfate, suggests that there may be an influence of the interaction of FGF4 with pericellular matrix and the dose-and time-dependence of the phosphorylation of FRS2α and MAPK1and MAPK3.
AbstractList Gradients of FGFs are an essential feature of many developmental processes. Thus, FGF2 stimulates different responses at high and low concentrations, while FGF4 gradients are critical, e.g., in limb development., but it is not known if responses to FGF4 differ in a concentration-dependent manner. Employing rat mammary (Rama) 27 fibroblasts, we therefore measured the FGF4 concentration- and time-dependence of the simulation of phosphorylation of FRS2α, MAPK1 and MAPK3 which are downstream of the FGF receptor (FGFR1c). At 10 pg/mL FGF4 caused a very weak phosphorylation of FRS2α at Y435 and Y196 and a stronger one of MAPK1 and MAPK3 that oscillated with maximum levels after 30 min and 240 min stimulation. The phosphorylation of these proteins at 1 ng/mL FGF4 was considerably stronger and showed a similar oscillation. At 10 ng/mL FGF4, the phosphorylation of FRS2α reached an early peak after 5 min, declined at 15 min and then rose again at 30 min before declining to the end of the time-course at 240 min, whereas the phosphorylation of MAPK1 and MAPK3 was strong after 5 minutes, reached a maximum after 30 minutes and then declined gradually. At 1 µg/mL and 3 µg/mL FGF4 after 15 min and 60 min the phosphorylation of FRS2α, MAPK1 and MAPK3 was much lower at 60 min compared to that observed at lower concentrations of FGF4. The data indicate that at low concentrations FGF4 elicits an oscillatory response at the level of phosphorylation of FRS2α and of MAPK1 and MAPK3, whereas a bell-shaped dose response may occur at the highest concentrations of FGF4. The addition of exogenous heparin, an effective mimic of endogenous heparan sulfate, suggests that there may be an influence of the interaction of FGF4 with pericellular matrix and the dose-and time-dependence of the phosphorylation of FRS2α and MAPK1and MAPK3.
Author Su, Dunhao
Fernig, David G.
Alsadun, Marim M.
Yates, Edwin A.
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  givenname: Marim M.
  surname: Alsadun
  fullname: Alsadun, Marim M.
  organization: Department of Biology, University of Tabuk
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  givenname: Dunhao
  orcidid: 0000-0002-9760-3419
  surname: Su
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  organization: Department of Biochemistry and Systems Biology, Institute of Molecular and Integrative Biology, University of Liverpool
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  surname: Yates
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  surname: Fernig
  fullname: Fernig, David G.
  email: dgfernig@liv.ac.uk
  organization: Department of Biochemistry and Systems Biology, Institute of Molecular and Integrative Biology, University of Liverpool
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Notes Competing Interest Statement: The authors have declared no competing interest.
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References Zhu (2025.05.09.652961v1.9) 2010; 8
Rudland, Davies, Tsao (2025.05.09.652961v1.25) 1984; 120
Nunes (2025.05.09.652961v1.3) 2016; 4
Turner, Grose (2025.05.09.652961v1.2) 2010; 10
Ke (2025.05.09.652961v1.21) 1990; 171
Alotaibi (2025.05.09.652961v1.34) 2024; 68
Cohn (2025.05.09.652961v1.24) 1995; 80
Wilcockson (2025.05.09.652961v1.33) 2023; 58
Zhang (2025.05.09.652961v1.11) 2008; 22
Fox (2025.05.09.652961v1.20) 1988; 263
Chai (2025.05.09.652961v1.12) 1998; 198
Delehedde (2025.05.09.652961v1.26) 2002; 366
Delehedde (2025.05.09.652961v1.27) 2000; 275
Li, Basilico, Mansukhani (2025.05.09.652961v1.19) 1994; 14
Ferguson, Smith, Francavilla (2025.05.09.652961v1.8) 2021; 10
Fernig, Smith, Rudland (2025.05.09.652961v1.32) 1990; 142
Rahmoune (2025.05.09.652961v1.29) 1998; 273
Goutam (2025.05.09.652961v1.1) 2023; 24
Ornitz (2025.05.09.652961v1.30) 1996; 271
Froese (2025.05.09.652961v1.35) 2024; 14
Serls (2025.05.09.652961v1.23) 2005; 132
Niswander (2025.05.09.652961v1.15) 2025; 521
Jackson (2025.05.09.652961v1.17) 2003; 17
Miura (2025.05.09.652961v1.13) 2018; 10
Marshall (2025.05.09.652961v1.28) 1995; 80
Duchesne (2025.05.09.652961v1.31) 2012; 10
Jackson, Koterwas, Bradford (2025.05.09.652961v1.16) 2006; 247
Zhang (2025.05.09.652961v1.10) 2006; 281
Tanaka (2025.05.09.652961v1.22) 1983; 11
Kuijk (2025.05.09.652961v1.18) 2012; 139
Sun (2025.05.09.652961v1.5) 2015; 3
Sun (2025.05.09.652961v1.4) 2016; 6
Lincoln, Alfieri, Yutzey (2025.05.09.652961v1.14) 2006; 292
Ornitz, Itoh (2025.05.09.652961v1.6) 2015; 4
Hadari (2025.05.09.652961v1.7) 2001; 98
References_xml – volume: 4
  start-page: 215
  issue: 3
  year: 2015
  end-page: 66
  ident: 2025.05.09.652961v1.6
  article-title: The Fibroblast Growth Factor signaling pathway
  publication-title: Wiley Interdiscip Rev Dev Biol
– volume: 247
  start-page: 183
  issue: 1-2
  year: 2006
  end-page: 91
  ident: 2025.05.09.652961v1.16
  article-title: Differential regulation of cell growth and gene expression by FGF-2 and FGF-4 in pituitary lactotroph GH4 cells
  publication-title: Mol Cell Endocrinol
– volume: 120
  start-page: 364
  issue: 3
  year: 1984
  end-page: 76
  ident: 2025.05.09.652961v1.25
  article-title: Rat mammary preadipocytes in culture produce a trophic agent for mammary epithelia-prostaglandin E2
  publication-title: J Cell Physiol
– volume: 142
  start-page: 108
  issue: 1
  year: 1990
  end-page: 16
  ident: 2025.05.09.652961v1.32
  article-title: Appearance of basic fibroblast growth factor receptors upon differentiation of rat mammary epithelial to myoepithelial-like cells in culture
  publication-title: J Cell Physiol
– volume: 68
  start-page: 479
  issue: 4
  year: 2024
  end-page: 489
  ident: 2025.05.09.652961v1.34
  article-title: Interactions of proteins with heparan sulfate
  publication-title: Essays Biochem
– volume: 14
  start-page: 32174
  issue: 1
  year: 2024
  ident: 2025.05.09.652961v1.35
  article-title: Evolution of SARS-CoV-2 spike trimers towards optimized heparan sulfate cross-linking and inter-chain mobility
  publication-title: Scientific Reports
– volume: 10
  start-page: 272
  issue: 1
  year: 2018
  end-page: 286
  ident: 2025.05.09.652961v1.13
  article-title: O-GlcNAc on PKCzeta Inhibits the FGF4-PKCzeta-MEK-ERK1/2 Pathway via Inhibition of PKCzeta Phosphorylation in Mouse Embryonic Stem Cells
  publication-title: Stem Cell Reports
– volume: 80
  start-page: 179
  issue: 2
  year: 1995
  end-page: 85
  ident: 2025.05.09.652961v1.28
  article-title: Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation
  publication-title: Cell
– volume: 366
  start-page: 235
  issue: Pt 1
  year: 2002
  end-page: 44
  ident: 2025.05.09.652961v1.26
  article-title: Fibroblast growth factor-2 binds to small heparin-derived oligosaccharides and stimulates a sustained phosphorylation of p42/44 mitogen-activated protein kinase and proliferation of rat mammary fibroblasts
  publication-title: Biochem J
– volume: 292
  start-page: 292
  issue: 2
  year: 2006
  end-page: 302
  ident: 2025.05.09.652961v1.14
  article-title: BMP and FGF regulatory pathways control cell lineage diversification of heart valve precursor cells
  publication-title: Dev Biol
– volume: 132
  start-page: 35
  issue: 1
  year: 2005
  end-page: 47
  ident: 2025.05.09.652961v1.23
  article-title: Different thresholds of fibroblast growth factors pattern the ventral foregut into liver and lung
  publication-title: Development
– volume: 80
  start-page: 739
  issue: 5
  year: 1995
  end-page: 46
  ident: 2025.05.09.652961v1.24
  article-title: Fibroblast growth factors induce additional limb development from the flank of chick embryos
  publication-title: Cell
– volume: 139
  start-page: 871
  issue: 5
  year: 2012
  end-page: 82
  ident: 2025.05.09.652961v1.18
  article-title: The roles of FGF and MAP kinase signaling in the segregation of the epiblast and hypoblast cell lineages in bovine and human embryos
  publication-title: Development
– volume: 275
  start-page: 33905
  issue: 43
  year: 2000
  end-page: 10
  ident: 2025.05.09.652961v1.27
  article-title: Fibroblast growth factor-2 stimulation of p42/44MAPK phosphorylation and IkappaB degradation is regulated by heparan sulfate/heparin in rat mammary fibroblasts
  publication-title: J Biol Chem
– volume: 11
  start-page: 1707
  issue: 6
  year: 1983
  end-page: 23
  ident: 2025.05.09.652961v1.22
  article-title: Expression in Escherichia coli of chemically synthesized gene for the human immune interferon
  publication-title: Nucleic Acids Res
– volume: 22
  start-page: 167
  issue: 1
  year: 2008
  end-page: 75
  ident: 2025.05.09.652961v1.11
  article-title: Fibroblast growth factor receptor 1 (FGFR1) tyrosine phosphorylation regulates binding of FGFR substrate 2alpha (FRS2alpha) but not FRS2 to the receptor
  publication-title: Mol Endocrinol
– volume: 521
  start-page: 149
  year: 2025
  end-page: 152
  ident: 2025.05.09.652961v1.15
  article-title: From the 1948 discovery of the apical ectodermal ridge in proximal-distal limb development to FGF molecular signals
  publication-title: Dev Biol
– volume: 98
  start-page: 8578
  issue: 15
  year: 2001
  end-page: 83
  ident: 2025.05.09.652961v1.7
  article-title: Critical role for the docking-protein FRS2 alpha in FGF receptor-mediated signal transduction pathways
  publication-title: Proc Natl Acad Sci U S A
– volume: 8
  start-page: 14
  year: 2010
  ident: 2025.05.09.652961v1.9
  article-title: The heparan sulfate co-receptor and the concentration of fibroblast growth factor-2 independently elicit different signalling patterns from the fibroblast growth factor receptor
  publication-title: Cell Commun Signal
– volume: 263
  start-page: 18452
  issue: 34
  year: 1988
  end-page: 8
  ident: 2025.05.09.652961v1.20
  article-title: Production, biological activity, and structure of recombinant basic fibroblast growth factor and an analog with cysteine replaced by serine
  publication-title: J Biol Chem
– volume: 4
  start-page: e1535
  year: 2016
  ident: 2025.05.09.652961v1.3
  article-title: Fibroblast growth factors as tissue repair and regeneration therapeutics
  publication-title: PeerJ
– volume: 273
  start-page: 7303
  issue: 13
  year: 1998
  end-page: 10
  ident: 2025.05.09.652961v1.29
  article-title: Interaction of heparan sulfate from mammary cells with acidic fibroblast growth factor (FGF) and basic FGF. Regulation of the activity of basic FGF by high and low affinity binding sites in heparan sulfate
  publication-title: J Biol Chem
– volume: 171
  start-page: 963
  issue: 3
  year: 1990
  end-page: 71
  ident: 2025.05.09.652961v1.21
  article-title: High-level production of human acidic fibroblast growth factor in E. coli cells: inhibition of DNA synthesis in rat mammary fibroblasts at high concentrations of growth factor
  publication-title: Biochem Biophys Res Commun
– volume: 198
  start-page: 105
  issue: 1
  year: 1998
  end-page: 15
  ident: 2025.05.09.652961v1.12
  article-title: FGF is an essential regulator of the fifth cell division in preimplantation mouse embryos
  publication-title: Dev Biol
– volume: 10
  start-page: e1001361
  issue: 7
  year: 2012
  ident: 2025.05.09.652961v1.31
  article-title: Transport of fibroblast growth factor 2 in the pericellular matrix is controlled by the spatial distribution of its binding sites in heparan sulfate
  publication-title: PLoS Biol
– volume: 58
  start-page: 2802
  issue: 23
  year: 2023
  end-page: 2818.e5
  ident: 2025.05.09.652961v1.33
  article-title: An improved Erk biosensor detects oscillatory Erk dynamics driven by mitotic erasure during early development
  publication-title: Developmental Cell
– volume: 17
  start-page: 1921
  issue: 10
  year: 2003
  end-page: 30
  ident: 2025.05.09.652961v1.17
  article-title: Fibroblast growth factors regulate prolactin transcription via an atypical Rac-dependent signaling pathway
  publication-title: Mol Endocrinol
– volume: 271
  start-page: 15292
  issue: 25
  year: 1996
  end-page: 7
  ident: 2025.05.09.652961v1.30
  article-title: Receptor specificity of the fibroblast growth factor family
  publication-title: J Biol Chem
– volume: 10
  start-page: 1201
  issue: 5
  year: 2021
  ident: 2025.05.09.652961v1.8
  article-title: Fibroblast Growth Factor Receptors (FGFRs) and Noncanonical Partners in Cancer Signaling
  publication-title: Cells
– volume: 281
  start-page: 15694
  issue: 23
  year: 2006
  end-page: 700
  ident: 2025.05.09.652961v1.10
  article-title: Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family
  publication-title: J Biol Chem
– volume: 14
  start-page: 7660
  issue: 11
  year: 1994
  end-page: 9
  ident: 2025.05.09.652961v1.19
  article-title: Cell transformation by fibroblast growth factors can be suppressed by truncated fibroblast growth factor receptors
  publication-title: Mol Cell Biol
– volume: 24
  issue: 8
  year: 2023
  ident: 2025.05.09.652961v1.1
  article-title: Exploring the Structural and Functional Diversity among FGF Signals: A Comparative Study of Human, Mouse, and Xenopus FGF Ligands in Embryonic Development and Cancer Pathogenesis
  publication-title: Int J Mol Sci
– volume: 10
  start-page: 116
  issue: 2
  year: 2010
  end-page: 29
  ident: 2025.05.09.652961v1.2
  article-title: Fibroblast growth factor signalling: from development to cancer
  publication-title: Nat Rev Cancer
– volume: 3
  start-page: e1060
  year: 2015
  ident: 2025.05.09.652961v1.5
  article-title: HaloTag is an effective expression and solubilisation fusion partner for a range of fibroblast growth factors
  publication-title: PeerJ
– volume: 6
  issue: 3
  year: 2016
  ident: 2025.05.09.652961v1.4
  article-title: Selectivity in glycosaminoglycan binding dictates the distribution and diffusion of fibroblast growth factors in the pericellular matrix
  publication-title: Open Biol
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Title Concentration- and time-dependence of phosphorylation events stimulated by fibroblast growth factor-4 (FGF-4) in Rama 27 fibroblasts
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