DOI: 10.1083/jcb.139.2.365. Dynamic Distribution of Chemoattractant Receptors in Living Cells During Chemotaxis and Persistent Stimulation

Dynamic Distribution of Chemoattractant Receptors in Living Cells During Chemotaxis and Persistent Stimulation

10.1083/jcb.139.2.365

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

While the localization of chemoattractant receptors on randomly oriented cells has been previously studied by immunohistochemistry, the instantaneous distribution of receptors on living cells undergoing directed migration has not been determined. To do this, we replaced cAR1, the primary cAMP receptor of Dictyostelium, with a cAR1-green fluorescence protein fusion construct. We found that this chimeric protein is functionally indistinguishable from wild-type cAR1. By time-lapse imaging of single cells, we observed that the receptors remained evenly distributed on the cell surface and all of its projections during chemotaxis involving turns and reversals of polarity directed by repositioning of a chemoattractant-filled micropipet. Thus, cell polarization cannot result from a gradient-induced asymmetric distribution of chemoattractant receptors. Some newly extended pseudopods at migration fronts showed a transient drop in fluorescence signals, suggesting that the flow of receptors into these zones may slightly lag behind the protrusion process. Challenge with a uniform increase in chemoattractant, sufficient to cause a dramatic decrease in the affinity of surface binding sites and cell desensitization, also did not significantly alter the distribution profile. Hence, the induced reduction in binding activity and cellular sensitivity cannot be due to receptor relocalization. The chimeric receptors were able to “cap” rapidly during treatment with Con A, suggesting that they are mobile in the plane of the cell membrane. This capping was not influenced by pretreatment with chemoattractant.

Bibliography

Xiao, Z., Zhang, N., Murphy, D. B., & Devreotes, P. N. (1997). Dynamic Distribution of Chemoattractant Receptors in Living Cells During Chemotaxis and Persistent Stimulation. The Journal of Cell Biology, 139(2), 365â374.

Authors 4

Zhan Xiao (first)
Ning Zhang (additional)
Douglas B. Murphy (additional)
Peter N. Devreotes (additional)

References 47 Referenced 193

10.1182/blood.V89.8.2670 / Blood / Human immunodeficiency virus (HIV)-resistant CD4+ UT-7 megakaryocytic human cell line becomes highly HIV-1 and HIV-2 susceptible upon CXCR4 transfection: induction of cell differentiation by HIV-1 infection by Baiocchi (1997)
10.1016/S0021-9258(17)42012-6 / J Biol Chem / A highly conserved tyrosine residue in G protein-coupled receptors is required for agonist-mediated β 2-adrenergic receptor sequestration by Barak (1994)
10.1016/0006-8993(94)91966-6 / Brain Res / Correlation of gp140trk expression and NGF-induced neuroblast chemotaxis in the embryonic rat spinal cord by Behar (1994)
10.1074/jbc.270.15.8667 / J Biol Chem / Agonist- induced loss of ligand binding is correlated with phosphorylation of cAR1, a G protein-coupled chemoattractant receptor from Dictyostelium. by Caterina (1995)
10.1006/bbrc.1995.2796 / Biochem Biophys Res Commun / Endothelin-1 induces rapid and long lasting internalization of the thrombin receptor in human glomerular epithelial cells by Chen (1995)
10.1016/0168-9525(96)81400-4 / Trends Genet / Signaling through chemoattractant receptors in Dictyostelium. by Chen (1996)
10.1016/S0165-6147(96)10048-1 / Trends Pharmacol Sci / G protein-coupled receptors: heterologous regulation of homologous desensitization and its implications by Chuang (1996)
10.1016/S0968-0004(00)89099-4 / Trends Biochem Sci / Understanding, improving and using green fluorescent proteins by Cubitt (1995)
{'key': '2023072823542861500_B9', 'first-page': '23', 'article-title': 'Capping of Con A receptors and actin distribution are influenced by disruption of microtubules in Dictyostelium discoideum.', 'volume': '51', 'author': 'de Priester', 'year': '1990', 'journal-title': 'Eur J Cell Biol'} / Eur J Cell Biol / Capping of Con A receptors and actin distribution are influenced by disruption of microtubules in Dictyostelium discoideum. by de Priester (1990)
10.1016/0896-6273(94)90267-4 / Neuron / G protein-linked signaling pathways control the developmental program of Dictyostelium. by Devreotes (1994)
10.1146/annurev.cb.04.110188.003245 / Annu Rev Cell Biol / Chemotaxis in eukaryotic cells: a focus on leukocytes and Dictyostelium. by Devreotes (1988)
{'key': '2023072823542861500_B12'}
10.1006/expr.1994.1104 / Exp Parasitol / Entamoeba histolytica: mechanism of surface receptor capping by Espinosa-Cantellano (1994)
10.1083/jcb.108.3.973 / J Cell Biol / Quantitative analysis of cell motility and chemotaxis in Dictyostelium discoideumby using an image processing system and a novel chemotaxis chamber providing stationary chemical gradients by Fisher (1989)
{'key': '2023072823542861500_B15', 'first-page': '319', 'article-title': 'Desensitization of G protein-coupled receptors', 'volume': '51', 'author': 'Freedman', 'year': '1996', 'journal-title': 'Recent Prog Horm Res'} / Recent Prog Horm Res / Desensitization of G protein-coupled receptors by Freedman (1996)
10.1242/jcs.52.1.1 / J Cell Sci / Chemotactic reorientation of granulocytes stimulated with micropipettes containing fMet-Leu-Phe by Gerisch (1981)
10.1098/rstb.1975.0080 / Philos Trans R Soc Lond B Biol Sci / Cell communication by periodic cyclic AMP pulses by Gerisch (1975)
10.1016/S0960-9822(95)00254-5 / Curr Biol / Chemoattractant-controlled accumulation of coronin at the leading edge of Dictyosteliumcells monitored using a green fluorescent protein-coronin fusion protein by Gerisch (1995)
10.1073/pnas.93.2.828 / Proc Natl Acad Sci USA / In vivo examination of membrane protein localization and degradation with green fluorescent protein by Hampton (1996)
10.1002/(SICI)1098-1128(199609)16:5<407::AID-MED2>3.0.CO;2-Z / Med Res Rev / Cellular and molecular mechanisms involved in the regulation of eosinophil trafficking in vivo by Hogan (1996)
10.1016/S0021-9258(18)31704-6 / J Biol Chem / Identification of a cytoplasmic Ser-Thr-Leu motif that determines agonist-induced internalization of the AT1 angiotensin receptor by Hunyady (1994)
10.1083/jcb.107.3.921 / J Cell Biol / Lateral segregation of neutrophil chemotactic receptors into actin- and fodrin-rich plasma membrane microdomains depleted in guanyl nucleotide regulatory proteins by Jesaitis (1988)
10.1083/jcb.109.6.2783 / J Cell Biol / Regulation of chemoattractant receptor interaction with transducing proteins by organizational control in the plasma membrane of human neutrophils by Jesaitis (1989)
10.1021/bi00242a025 / Biochemistry / Overexpression of the cAMP receptor 1 in growing Dictyosteliumcells by Johnson (1991)
10.1016/S0021-9258(18)42875-X / J Biol Chem / The cyclic nucleotide specificity of three cAMP receptors in Dictyostelium. by Johnson (1992)
10.1016/S0021-9258(19)61965-4 / J Biol Chem / Random chimeragenesis of G protein-coupled receptors. Mapping the affinity of the cAMP chemoattractant receptors in Dictyostelium. by Kim (1994)
10.1016/S0021-9258(18)89658-2 / J Biol Chem / Identification and cyclic AMP-induced modification of the cyclic AMP receptor in Dictyostelium discoideum. by Klein (1985)
{'key': '2023072823542861500_B28'}
10.1016/0006-2952(94)90439-1 / Biochem Pharmacol / Agonist-induced muscarinic cholinergic receptor internalization, recycling and degradation in cultured neuronal cells. Cellular mechanisms and role in desensitization by Maloteaux (1994)
10.1016/0092-8674(95)90207-4 / Cell / Coronin involved in phagocytosis: dynamics of particle-induced relocalization visualized by a green fluorescent protein Tag by Maniak (1995)
10.1016/0896-6273(95)90279-1 / Neuron / The jellyfish green fluorescent protein: a new tool for studying ion channel expression and function by Marshall (1995)
10.1002/elps.1150110116 / Electrophoresis / Analysis of plasma membrane protein changes in Dictyostelium discoideumduring concanavalin A induced receptor redistribution using two-dimensional gel electrophoresis by Patton (1990)
10.1073/pnas.83.12.4332 / Proc Natl Acad Sci USA / Polymorphonuclear leukocyte histamine receptors: occurrence in cell surface clusters and their redistribution during locomotion by Petty (1986)
{'key': '2023072823542861500_B34'}
10.1074/jbc.271.32.19186 / J Biol Chem / Role of the C terminus of the interleukin 8 receptor in signal transduction and internalization by Prado (1996)
10.1111/j.1768-322X.1987.tb00551.x / Biol Cell / Redistribution of muscarinic acetylcholine receptors on human fibroblasts induced by regulatory ligands by Raposo (1987)
10.1083/jcb.128.6.1029 / J Cell Biol / Dual pathways of internalization of the cholecystokinin receptor by Roettger (1995)
10.1083/jcb.130.3.579 / J Cell Biol / Insulation of a G protein-coupled receptor on the plasmalemmal surface of the pancreatic acinar cell by Roettger (1995)
10.1016/S0092-8674(00)81068-5 / Cell / ord-10 encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl by Sengupta (1996)
{'key': '2023072823542861500_B40', 'first-page': '201', 'article-title': 'Effect of obstructive cholestasis on membrane traffic and domain-specific expression of plasma membrane proteins in rat liver parenchymal cells', 'volume': '20', 'author': 'Stieger', 'year': '1994', 'journal-title': 'Hepatology'} / Hepatology / Effect of obstructive cholestasis on membrane traffic and domain-specific expression of plasma membrane proteins in rat liver parenchymal cells by Stieger (1994)
10.1096/fasebj.9.9.7601339 / FASEB J / The family of G-protein-coupled receptors by Strader (1995)
10.1016/0092-8674(82)90340-3 / Cell / Local and spatially coordinated movements in Dictyostelium discoideumamoebae during chemotaxis by Swanson (1982)
10.1159/000163891 / Pathobiology / Interleukin-8 and tumor necrosis factor-α are involved in human aortic endothelial cell migration. The possible role of these cytokines in human aortic aneurysmal blood vessel growth by Szekanecz (1994)
10.1016/S0021-9258(19)50762-1 / J Biol Chem / Ligand-regulated internalization and recycling of human β 2-adrenergic receptors between the plasma membrane and endosomes containing transferrin receptors by von Zastrow (1992)
10.1016/0012-1606(88)90268-0 / Dev Biol / Localization of chemoattractant receptors on Dictyostelium discoideumcells during aggregation and down-regulation by Wang (1988)
10.1016/S1074-5521(96)90126-X / Chem Biol / Chemokine receptors: the new frontier for AIDS research by Wells (1996)
10.1091/mbc.8.5.855 / Mol Biol Cell / Identification of detergent-resistant plasma membrane microdomains in Dictyostelium: enrichment of signal transduction proteins by Xiao (1997)

Dates

Type	When
Created	23 years, 1 month ago (July 26, 2002, 12:47 p.m.)
Deposited	2 years ago (July 28, 2023, 7:55 p.m.)
Indexed	2 weeks, 6 days ago (Aug. 6, 2025, 9:51 a.m.)
Issued	27 years, 10 months ago (Oct. 20, 1997)
Published	27 years, 10 months ago (Oct. 20, 1997)
Published Online	27 years, 10 months ago (Oct. 20, 1997)
Published Print	27 years, 10 months ago (Oct. 20, 1997)

Funders 0

None

BibTeX

@article{Xiao_1997, title={Dynamic Distribution of Chemoattractant Receptors in Living Cells During Chemotaxis and Persistent Stimulation}, volume={139}, ISSN={1540-8140}, url={http://dx.doi.org/10.1083/jcb.139.2.365}, DOI={10.1083/jcb.139.2.365}, number={2}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Xiao, Zhan and Zhang, Ning and Murphy, Douglas B. and Devreotes, Peter N.}, year={1997}, month=oct, pages={365–374} }

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      "first-page": "8667",
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      "article-title": "Agonist- induced loss of ligand binding is correlated with phosphorylation of cAR1, a G protein-coupled chemoattractant receptor from Dictyostelium.",
      "volume": "270",
      "author": "Caterina",
      "year": "1995",
      "journal-title": "J Biol Chem"
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    {
      "key": "2023072823542861500_B5",
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      "first-page": "445",
      "DOI": "10.1006/bbrc.1995.2796",
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      "volume": "217",
      "author": "Chen",
      "year": "1995",
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      "article-title": "Signaling through chemoattractant receptors in Dictyostelium.",
      "volume": "12",
      "author": "Chen",
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      "journal-title": "Trends Genet"
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    {
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