Chemotactic signaling in mesenchymal cells compared to amoeboid cells

Genes and Diseases

Volumn 1, Issue 2, 2014, Pages 162-173

  Vorotnikov, Alexander V ^a,b   Tyurin Kuzmin, Pyotr A ^a  

^a LOMONOSOV MOSCOW STATE UNIVERSITY   (Russian Federation)

^b INSTITUTE OF EXPERIMENTAL CARDIOLOGY   (Russian Federation)

Author keywords

Chemotaxis; Feedback regulation; Fibroblasts; Hydrogen peroxide; Signaling

Indexed keywords

G PROTEIN COUPLED RECEPTOR; PHOSPHOLIPASE A2; PROTEIN TYROSINE KINASE;

ADAPTATION; AMOEBOID CELL; CELL MIGRATION; CELL MOTILITY; CELL STRUCTURE; CELL TYPE; CHEMOTAXIS; CYTOSKELETON; FEEDBACK SYSTEM; INTRACELLULAR SIGNALING; MESENCHYME CELL; REVIEW;

EID: 84978154031     PISSN: None     EISSN: 23523042     Source Type: Journal    
DOI: 10.1016/j.gendis.2014.09.006     Document Type: Review

References (103)

1. King J.S., Insall R.H. Chemotaxis: finding the way forward with Dictyostelium. Trends Cell Biol Oct 2009, 19:523-530.
2. Swaney K.F., Huang C.H., Devreotes P.N. Eukaryotic chemotaxis: a network of signaling pathways controls motility, directional sensing, and polarity. Annu Rev Biophys Jun 9 2010, 39:265-289.
3. von Philipsborn A., Bastmeyer M. Mechanisms of gradient detection: a comparison of axon pathfinding with eukaryotic cell migration. Int Rev Cytol 2007, 263:1-62.
4. Vorotnikov A.V. Chemotaxis: movement, direction, control. Biochemistry (Mosc) Dec 2011, 76:1528-1555.
5. Xiong Y., Huang C.H., Iglesias P.A., Devreotes P.N. Cells navigate with a local-excitation, global-inhibition-biased excitable network. Proc Natl Acad Sci U S A Oct 5 2010, 107:17079-17086.
6. Pankov R., Endo Y., Even-Ram S., et al. A Rac switch regulates random versus directionally persistent cell migration. J Cell Biol Aug 29 2005, 170:793-802.
7. Jiang X., Bruzewicz D.A., Wong A.P., Piel M., Whitesides G.M. Directing cell migration with asymmetric micropatterns. Proc Natl Acad Sci U S A Jan 25 2005, 102:975-978.
8. Annesley S.J., Fisher P.R. Dictyostelium discoideum - a model for many reasons. Mol Cell Biochem Sep 2009, 329:73-91.
9. Drayer A.L., van Haastert P.J. Transmembrane signalling in eukaryotes: a comparison between higher and lower eukaryotes. Plant Mol Biol Dec 1994, 26:1239-1270.
10. Shaw T.J., Martin P. Wound repair at a glance. J Cell Sci Sep 15 2009, 122:3209-3213.
11. Irie H.Y., Pearline R.V., Grueneberg D., et al. Distinct roles of Akt1 and Akt2 in regulating cell migration and epithelial-mesenchymal transition. J Cell Biol Dec 19 2005, 171:1023-1034.
12. Abercrombie M. The crawling movement of metazoan cells. The Croonian lecture 1978. Proc R Soc Lond B Biol Sci 1980, 207:129-147.
13. Haugh J.M., Codazzi F., Teruel M., Meyer T. Spatial sensing in fibroblasts mediated by 3' phosphoinositides. J Cell Biol Dec 11 2000, 151:1269-1280.
14. Small J.V., Anderson K., Rottner K. Actin and the coordination of protrusion, attachment and retraction in cell crawling. Biosci Rep Oct 1996, 16:351-368.
15. Devreotes P.N., Zigmond S.H. Chemotaxis in eukaryotic cells: a focus on leukocytes and Dictyostelium. Annu Rev Cell Biol 1988, 4:649-686.
16. Schneider I.C., Haugh J.M. Mechanisms of gradient sensing and chemotaxis: conserved pathways, diverse regulation. Cell Cycle Jun 2006, 5:1130-1134.
17. De Bruyn P.P. The amoeboid movement of the mammalian leukocyte in tissue culture. Anat Rec Jun 1946, 95:177-191.
18. Weijer C.J. Dictyostelium morphogenesis. Curr Opin Genet Dev Aug 2004, 14:392-398.
19. Chisholm R.L., Gaudet P., Just E.M., et al. dictyBase, the model organism database for Dictyostelium discoideum. Nucleic Acids Res Jan 1 2006, 34:D423-D427.
20. Niggli V. Signaling to migration in neutrophils: importance of localized pathways. Int J Biochem Cell Biol Dec 2003, 35:1619-1638.
21. Foxman E.F., Kunkel E.J., Butcher E.C. Integrating conflicting chemotactic signals. The role of memory in leukocyte navigation. J Cell Biol Nov 1 1999, 147:577-588.
22. Zigmond S.H. Ability of polymorphonuclear leukocytes to orient in gradients of chemotactic factors. J Cell Biol Nov 1977, 75:606-616.
23. Andrew N., Insall R.H. Chemotaxis in shallow gradients is mediated independently of PtdIns 3-kinase by biased choices between random protrusions. Nat Cell Biol Feb 2007, 9:193-200.
24. Bosgraaf L., Van Haastert P.J. Navigation of chemotactic cells by parallel signaling to pseudopod persistence and orientation. PLoS One 2009, 4:e6842.
25. Puck T.T., Cieciura S.J., Fisher H.W. Clonal growth invitro of human cells with fibroblastic morphology; comparison of growth and genetic characteristics of single epithelioid and fibroblast-like cells from a variety of human organs. J Exp Med Jul 1 1957, 106:145-158.
26. Lauffenburger D.A., Horwitz A.F. Cell migration: a physically integrated molecular process. Cell Feb 9 1996, 84:359-369.
27. Friedl P. Prespecification and plasticity: shifting mechanisms of cell migration. Curr Opin Cell Biol Feb 2004, 16:14-23.
28. Deuel T.F., Kawahara R.S., Mustoe T.A., Pierce A.F. Growth factors and wound healing: platelet-derived growth factor as a model cytokine. Annu Rev Med 1991, 42:567-584.
29. De Donatis A., Comito G., Buricchi F., et al. Proliferation versus migration in platelet-derived growth factor signaling: the key role of endocytosis. J Biol Chem Jul 18 2008, 283:19948-19956.
30. Wiesner S., Legate K.R., Fassler R. Integrin-actin interactions. Cell Mol Life Sci May 2005, 62:1081-1099.
31. Woodham E.F., Machesky L.M. Polarised cell migration: intrinsic and extrinsic drivers. Curr Opin Cell Biol Jun 19 2014, 30C:25-32.
32. Schneider I.C., Haugh J.M. Quantitative elucidation of a distinct spatial gradient-sensing mechanism in fibroblasts. J Cell Biol Dec 5 2005, 171:883-892.
33. Shestakova E.A., Singer R.H., Condeelis J. The physiological significance of beta-actin mRNA localization in determining cell polarity and directional motility. Proc Natl Acad Sci U S A Jun 19 2001, 98:7045-7050.
34. Haugh J.M. Deterministic model of dermal wound invasion incorporating receptor-mediated signal transduction and spatial gradient sensing. Biophys J Apr 1 2006, 90:2297-2308.
35. Kawada K., Upadhyay G., Ferandon S., et al. Cell migration is regulated by platelet-derived growth factor receptor endocytosis. Mol Cell Biol Aug 2009, 29:4508-4518.
36. Vasiliev J.M. Cytoskeletal mechanisms responsible for invasive migration of neoplastic cells. Int J Dev Biol 2004, 48:425-439.
37. Bershadsky A., Kozlov M., Geiger B. Adhesion-mediated mechanosensitivity: a time to experiment, and a time to theorize. Curr Opin Cell Biol Oct 2006, 18:472-481.
38. Mitchison T.J., Cramer L.P. Actin-based cell motility and cell locomotion. Cell Feb 9 1996, 84:371-379.
39. Ridley A.J., Schwartz M.A., Burridge K., et al. Cell migration: integrating signals from front to back. Science Dec 5 2003, 302:1704-1709.
40. Small J.V., Geiger B., Kaverina I., Bershadsky A. How do microtubules guide migrating cells?. Nat Rev Mol Cell Biol Dec 2002, 3:957-964.
41. Pollard T.D., Borisy G.G. Cellular motility driven by assembly and disassembly of actin filaments. Cell Feb 21 2003, 112:453-465.
42. Carlier M.F., Pantaloni D. Control of actin assembly dynamics in cell motility. J Biol Chem Aug 10 2007, 282:23005-23009.
43. Cramer L.P. Mechanism of cell rear retraction in migrating cells. Curr Opin Cell Biol Oct 2013, 25:591-599.
44. Fournier M.F., Sauser R., Ambrosi D., Meister J.J., Verkhovsky A.B. Force transmission in migrating cells. J Cell Biol Jan 25 2010, 188:287-297.
45. Bershadsky A.D., Balaban N.Q., Geiger B. Adhesion-dependent cell mechanosensitivity. Annu Rev Cell Dev Biol 2003, 19:677-695.
46. Gardel M.L., Schneider I.C., Aratyn-Schaus Y., Waterman C.M. Mechanical integration of actin and adhesion dynamics in cell migration. Annu Rev Cell Dev Biol Nov 10 2010, 26:315-333.
47. Chrzanowska-Wodnicka M., Burridge K. Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J Cell Biol Jun 1996, 133:1403-1415.
48. Friedl P., Brocker E.B. The biology of cell locomotion within three-dimensional extracellular matrix. Cell Mol Life Sci Jan 20 2000, 57:41-64.
49. Friedl P., Wolf K. Plasticity of cell migration: a multiscale tuning model. J Cell Biol Jan 11 2010, 188:11-19.
50. Lammermann T., Sixt M. Mechanical modes of 'amoeboid' cell migration. Curr Opin Cell Biol Oct 2009, 21:636-644.
51. Charras G., Paluch E. Blebs lead the way: how to migrate without lamellipodia. Nat Rev Mol Cell Biol Sep 2008, 9:730-736.
52. Lammermann T., Bader B.L., Monkley S.J., et al. Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature May 1 2008, 453:51-55.
53. Renkawitz J., Schumann K., Weber M., et al. Adaptive force transmission in amoeboid cell migration. Nat Cell Biol Dec 2009, 11:1438-1443.
54. Xiao Z., Zhang N., Murphy D.B., Devreotes P.N. Dynamic distribution of chemoattractant receptors in living cells during chemotaxis and persistent stimulation. J Cell Biol Oct 20 1997, 139:365-374.
55. Servant G., Weiner O.D., Herzmark P., Balla T., Sedat J.W., Bourne H.R. Polarization of chemoattractant receptor signaling during neutrophil chemotaxis. Science Feb 11 2000, 287:1037-1040.
56. Janetopoulos C., Jin T., Devreotes P. Receptor-mediated activation of heterotrimeric G-proteins in living cells. Science Mar 23 2001, 291:2408-2411.
57. Jin T., Zhang N., Long Y., Parent C.A., Devreotes P.N. Localization of the G protein betagamma complex in living cells during chemotaxis. Science Feb 11 2000, 287:1034-1036.
58. Anand-Apte B., Zetter B. Signaling mechanisms in growth factor-stimulated cell motility. Stem Cells 1997, 15:259-267.
59. Xu J., Wang F., Van Keymeulen A., et al. Divergent signals and cytoskeletal assemblies regulate self-organizing polarity in neutrophils. Cell Jul 25 2003, 114:201-214.
60. Chudakov D.M., Matz M.V., Lukyanov S., Lukyanov K.A. Fluorescent proteins and their applications in imaging living cells and tissues. Physiol Rev Jul 2010, 90:1103-1163.
61. Pertz O. Spatio-temporal Rho GTPase signaling - where are we now?. J Cell Sci Jun 1 2010, 123:1841-1850.
62. Hawkins P.T., Anderson K.E., Davidson K., Stephens L.R. Signalling through class I PI3Ks in mammalian cells. Biochem Soc Trans Nov 2006, 34:647-662.
63. Parent C.A., Blacklock B.J., Froehlich W.M., Murphy D.B., Devreotes P.N. G protein signaling events are activated at the leading edge of chemotactic cells. Cell Oct 2 1998, 95:81-91.
64. Welch H.C., Coadwell W.J., Stephens L.R., Hawkins P.T. Phosphoinositide 3-kinase-dependent activation of Rac. FEBS Lett Jul 3 2003, 546:93-97.
65. Bosgraaf L., Russcher H., Smith J.L., Wessels D., Soll D.R., Van Haastert P.J. A novel cGMP signalling pathway mediating myosin phosphorylation and chemotaxis in Dictyostelium. Embo J Sep 2 2002, 21:4560-4570.
66. Grandoch M., Roscioni S.S., Schmidt M. The role of Epac proteins, novel cAMP mediators, in the regulation of immune, lung and neuronal function. Br J Pharmacol Jan 1 2010, 159:265-284.
67. Liu L., Das S., Losert W., Parent C.A. mTORC2 regulates neutrophil chemotaxis in a cAMP- and RhoA-dependent fashion. Dev Cell Dec 14 2010, 19:845-857.
68. Weiger M.C., Wang C.C., Krajcovic M., Melvin A.T., Rhoden J.J., Haugh J.M. Spontaneous phosphoinositide 3-kinase signaling dynamics drive spreading and random migration of fibroblasts. J Cell Sci Feb 1 2009, 122:313-323.
69. Van Haastert P.J., Devreotes P.N. Chemotaxis: signalling the way forward. Nat Rev Mol Cell Biol Aug 2004, 5:626-634.
70. Bosgraaf L., Van Haastert P.J. A model for cGMP signal transduction in Dictyostelium in perspective of 25 years of cGMP research. J Muscle Res Cell Motil 2002, 23:781-791.
71. Fincham V.J., James M., Frame M.C., Winder S.J. Active ERK/MAP kinase is targeted to newly forming cell-matrix adhesions by integrin engagement and v-Src. Embo J Jun 15 2000, 19:2911-2923.
72. Geiger B., Yamada K.M. Molecular architecture and function of matrix adhesions. Cold Spring Harb Perspect Biol 2011, 3(5).
73. Rericha E.C., Parent C.A. Steering in quadruplet: the complex signaling pathways directing chemotaxis. Sci Signal 2008, 1:pe26.
74. Hoeller O., Kay R.R. Chemotaxis in the absence of PIP3 gradients. Curr Biol May 1 2007, 17:813-817.
75. Chen L., Iijima M., Tang M., et al. PLA2 and PI3K/PTEN pathways act in parallel to mediate chemotaxis. Dev Cell Apr 2007, 12:603-614.
76. Zhou H., Huang S. Role of mTOR signaling in tumor cell motility, invasion and metastasis. Curr Protein Pept Sci Feb 2011, 12:30-42.
77. Laplante M., Sabatini D.M. mTOR signaling in growth control and disease. Cell Apr 13 2012, 149:274-293.
78. Cai H., Das S., Kamimura Y., Long Y., Parent C.A., Devreotes P.N. Ras-mediated activation of the TORC2-PKB pathway is critical for chemotaxis. J Cell Biol Jul 26 2010, 190:233-245.
79. Karsenti E. Self-organization in cell biology: a brief history. Nat Rev Mol Cell Biol Mar 2008, 9:255-262.
80. Bosgraaf L., Van Haastert P.J. The ordered extension of pseudopodia by amoeboid cells in the absence of external cues. PLoS One 2009, 4:e5253.
81. Weiger M.C., Ahmed S., Welf E.S., Haugh J.M. Directional persistence of cell migration coincides with stability of asymmetric intracellular signaling. Biophys J Jan 6 2010, 98:67-75.
82. Hurd T.R., Degennaro M., Lehmann R. Redox regulation of cell migration and adhesion. Trends Cell Biol Feb 2012, 22:107-115.
83. Stone J.R., Yang S. Hydrogen peroxide: a signaling messenger. Antioxid Redox Signal Mar-Apr 2006, 8:243-270.
84. Geiszt M., Leto T.L. The Nox family of NAD(P)H oxidases: host defense and beyond. J Biol Chem Dec 10 2004, 279:51715-51718.
85. Tyurin-Kuzmin P.A., Agaronian K.M., Morozov IaI., Mishina N.M., Belousov V.V., Vorotnikov A.V. NADPH oxidase controls EGF-induced proliferation via the ERK1/2-independent mechanism. Biofizika Nov-Dec 2010, 55:959-965.
86. Rocic P., Lucchesi P.A. NAD(P)H oxidases and TGF-beta-induced cardiac fibroblast differentiation: Nox-4 gets Smad. Circ Res Oct 28 2005, 97:850-852.
87. Bedard K., Krause K.H. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev Jan 2007, 87:245-313.
88. Ushio-Fukai M. Redox signaling in angiogenesis: role of NADPH oxidase. Cardiovasc Res Jul 15 2006, 71:226-235.
89. 2 for platelet-derived growth factor signal transduction. Science Oct 13 1995, 270:296-299.
90. San Martin A., Griendling K.K. Redox control of vascular smooth muscle migration. Antioxid Redox Signal Mar 1 2010, 12:625-640.
91. Niethammer P., Grabher C., Look A.T., Mitchison T.J. A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature Jun 18 2009, 459:996-999.
92. Brzostowski J.A., Sawai S., Rozov O., et al. Phosphorylation of chemoattractant receptors regulates chemotaxis, actin reorganization and signal relay. J Cell Sci Oct 15 2013, 126:4614-4626.
93. Rhee S.G., Bae Y.S., Lee S.R., Kwon J. Hydrogen peroxide: a key messenger that modulates protein phosphorylation through cysteine oxidation. Sci STKE Oct 10 2000, 2000:PE1.
94. Finkel T. Oxidant signals and oxidative stress. Curr Opin Cell Biol Apr 2003, 15:247-254.
95. Mishina N.M., Tyurin-Kuzmin P.A., Markvicheva K.N., et al. Does cellular hydrogen peroxide diffuse or act locally?. Antioxid Redox Signal Jan 1 2011, 14:1-7.
96. Droge W. Free radicals in the physiological control of cell function. Physiol Rev Jan 2002, 82:47-95.
97. Tonks N.K. Redox redux: revisiting PTPs and the control of cell signaling. Cell Jun 3 2005, 121:667-670.
98. den Hertog J., Groen A., van der Wijk T. Redox regulation of protein-tyrosine phosphatases. Arch Biochem Biophys Feb 1 2005, 434:11-15.
99. Kwon J., Lee S.R., Yang K.S., et al. Reversible oxidation and inactivation of the tumor suppressor PTEN in cells stimulated with peptide growth factors. Proc Natl Acad Sci U S A Nov 23 2004, 101:16419-16424.
100. McCubrey J.A., Steelman L.S., Chappell W.H., et al. Ras/Raf/MEK/ERK and PI3K/PTEN/Akt/mTOR cascade inhibitors: how mutations can result in therapy resistance and how to overcome resistance. Oncotarget Oct 2012, 3:1068-1111.
101. Kim J.S., Huang T.Y., Bokoch G.M. Reactive oxygen species regulate a slingshot-cofilin activation pathway. Mol Biol Cell Jun 2009, 20:2650-2660.
102. Lassing I., Schmitzberger F., Bjornstedt M., et al. Molecular and structural basis for redox regulation of beta-actin. J Mol Biol Jul 6 2007, 370:331-348.
103. Hung R.J., Pak C.W., Terman J.R. Direct redox regulation of F-actin assembly and disassembly by Mical. Science Dec 23 2011, 334:1710-1713.