1932

Abstract

Most single animal cells have an internal vector that determines where recycling membrane is added to the cell's surface. Because of the specific molecular composition of this added membrane, a dynamic asymmetry is formed on the surface of the cell. The consequences of this dynamic asymmetry are discussed, together with what they imply for how cells move. The polarity of a single-celled embryo, such as that of the nematode , is explored in a similar framework.

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2014-06-02
2024-05-04
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Literature Cited

  1. Marcus PI.1.  1962. Dynamics of surface modification in myxovirus-infected cells. Cold Spring Harb. Symp. Quant. Biol. 27:351–65 [Google Scholar]
  2. Pearse BM, Robinson MS. 2.  1990. Clathrin, adaptors, and sorting. Annu. Rev. Cell Biol. 6:151–71 [Google Scholar]
  3. Anderson RG, Goldstein JL, Brown MS. 3.  1976. Localization of low density lipoprotein receptors on plasma membrane of normal human fibroblasts and their absence in cells from a familial hypercholesterolemia homozygote. Proc. Natl. Acad. Sci. USA 73:2434–38 [Google Scholar]
  4. Bleil JD, Bretscher MS. 4.  1982. Transferrin receptor and its recycling in HeLa cells. EMBO J. 1:351–55 [Google Scholar]
  5. Bretscher MS, Thomson JN, Pearse BM. 5.  1980. Coated pits act as molecular filters. Proc. Natl. Acad. Sci. USA 77:4156–59 [Google Scholar]
  6. Bretscher MS.6.  1983. Distribution of receptors for transferrin and low density lipoprotein on the surface of giant HeLa cells. Proc. Natl. Acad. Sci. USA 80:454–58 [Google Scholar]
  7. Bretscher MS, Thomson JN. 7.  1983. Distribution of ferritin receptors and coated pits on giant HeLa cells. EMBO J. 2:599–603 [Google Scholar]
  8. Hopkins CR, Gibson A, Shipman M, Strickland DK, Trowbridge IS. 8.  1994. In migrating fibroblasts, recycling receptors are concentrated in narrow tubules in the pericentriolar area, and then routed to the plasma membrane of the leading lamella. J. Cell Biol. 125:1265–74 [Google Scholar]
  9. Marco E, Wedlich-Soldner R, Li R, Altschuler SJ, Wu LF. 9.  2007. Endocytosis optimizes the dynamic localization of membrane proteins that regulate cortical polarity. Cell 129:411–22 [Google Scholar]
  10. Bretscher MS.10.  1976. Directed lipid flow in cell membranes. Nature 260:21–23 [Google Scholar]
  11. Taylor RB, Duffus WPH, Raff MC, de Petris S. 11.  1971. Redistribution and pinocytosis of lymphocyte surface immunoglobulin molecules induced by an anti-immunoglobulin antibody. Nat. New Biol. 233:225–29 [Google Scholar]
  12. Stern PL, Bretscher MS. 12.  1979. Capping of exogenous Forssman glycolipid on cells. J. Cell Biol. 82:829–33 [Google Scholar]
  13. Abercrombie M, Heaysman JE, Pegrum SM. 13.  1970. The locomotion of fibroblasts in culture. 3. Movements of particles on the dorsal surface of the leading lamella. Exp. Cell Res. 62:389–98 [Google Scholar]
  14. Valdez-Taubas J, Pelham HR. 14.  2003. Slow diffusion of proteins in the yeast plasma membrane allows polarity to be maintained by endocytic cycling. Curr. Biol. 13:1636–40 [Google Scholar]
  15. Pruyne DW, Schott DH, Bretscher A. 15.  1998. Tropomyosin-containing actin cables direct the Myo2p-dependent polarized delivery of secretory vesicles in budding yeast. J. Cell Biol. 143:1931–45 [Google Scholar]
  16. Pollard TD, Borisy GG. 16.  2003. Cellular motility driven by assembly and disassembly of actin filaments. Cell 112:453–65 [Google Scholar]
  17. Pollard TD, Cooper JA. 17.  2009. Actin, a central player in cell shape and movement. Science 326:1208–12 [Google Scholar]
  18. Tilney LG, Portnoy DA. 18.  1989. Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J. Cell Biol. 109:1597–608 [Google Scholar]
  19. Wang YL.19.  1985. Exchange of actin subunits at the leading edge of living fibroblasts: possible role of treadmilling. J. Cell Biol. 101:597–602 [Google Scholar]
  20. Ridley AJ.20.  2011. Life at the leading edge. Cell 145:1012–22 [Google Scholar]
  21. Hynes RO.21.  1987. Integrins: a family of cell surface receptors. Cell 48:549–54 [Google Scholar]
  22. Bretscher MS.22.  1984. Endocytosis: relation to capping and cell locomotion. Science 224:681–86 [Google Scholar]
  23. Bretscher MS.23.  1992. Circulating integrins: α5β1, α6β4 and Mac-1, but not α3β1, α4β1 or LFA-1. EMBO J. 11:405–10 [Google Scholar]
  24. Bretscher MS.24.  1989. Endocytosis and recycling of the fibronectin receptor in CHO cells. EMBO J. 8:1341–48 [Google Scholar]
  25. Caswell PT, Norman JC. 25.  2006. Integrin trafficking and the control of cell migration. Traffic 7:14–21 [Google Scholar]
  26. De Deyne PG, O'Neill A, Resneck WG, Dmytrenko GM, Pumplin DW, Bloch RJ. 26.  1998. The vitronectin receptor associates with clathrin-coated membrane domains via the cytoplasmic domain of its β5 subunit. J. Cell Sci. 111:2729–40 [Google Scholar]
  27. Nishimura T, Kaibuchi K. 27.  2007. Numb controls integrin endocytosis for directional cell migration with aPKC and PAR-3. Dev. Cell 13:15–28 [Google Scholar]
  28. Ramsay AG, Keppler MD, Jazayeri M, Thomas GJ, Parsons M. 28.  et al. 2007. HS1-associated protein X-1 regulates carcinoma cell migration and invasion via clathrin-mediated endocytosis of integrin αvβ6. Cancer Res. 67:5275–84 [Google Scholar]
  29. Pierini LM, Lawson MA, Eddy RJ, Hendey B, Maxfield FR. 29.  2000. Oriented endocytic recycling of α5β1 in motile neutrophils. Blood 95:2471–80 [Google Scholar]
  30. Bretscher MS.30.  2008. On the shape of migrating cells—a ‘front-to-back’ model. J. Cell Sci. 121:2625–28 [Google Scholar]
  31. Brown MS, Goldstein JL. 31.  1979. Receptor-mediated endocytosis: insights from the lipoprotein receptor system. Proc. Natl. Acad. Sci. USA 76:3330–37 [Google Scholar]
  32. Taylor MJ, Perrais D, Merrifield CJ. 32.  2011. A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biol. 9:e1000604 [Google Scholar]
  33. Abercrombie M, Heaysman JE, Pegrum SM. 33.  1970. The locomotion of fibroblasts in culture. I. Movements of the leading edge. Exp. Cell Res. 59:393–98 [Google Scholar]
  34. Yang Y, Borset M, Langford JK, Sanderson RD. 34.  2003. Heparan sulfate regulates targeting of syndecan-1 to a functional domain on the cell surface. J. Biol. Chem. 278:12888–93 [Google Scholar]
  35. Bass MD, Williamson RC, Nunan RD, Humphries JD, Byron A. 35.  et al. 2011. A syndecan-4 hair trigger initiates wound healing through caveolin- and RhoG-regulated integrin endocytosis. Dev. Cell 21:681–93 [Google Scholar]
  36. Barry NP, Bretscher MS. 36.  2010. Dictyostelium amoebae and neutrophils can swim. Proc. Natl. Acad. Sci. USA 107:11376–80 [Google Scholar]
  37. Purcell EM.37.  1977. Life at low Reynolds number. Am. J. Phys. 45:3–11 [Google Scholar]
  38. Pruyne D, Legesse-Miller A, Gao L, Dong Y, Bretscher A. 38.  2004. Mechanisms of polarized growth and organelle segregation in yeast. Annu. Rev. Cell Dev. Biol. 20:559–91 [Google Scholar]
  39. Chibalina MV, Puri C, Kendrick-Jones J, Buss F. 39.  2009. Potential roles of myosin VI in cell motility. Biochem. Soc. Trans. 37:966–70 [Google Scholar]
  40. Schuh M.40.  2011. An actin-dependent mechanism for long-range vesicle transport. Nat. Cell Biol. 13:1431–36 [Google Scholar]
  41. Schmoranzer J, Kreitzer G, Simon SM. 41.  2003. Migrating fibroblasts perform polarized, microtubule-dependent exocytosis towards the leading edge. J. Cell Sci. 116:4513–19 [Google Scholar]
  42. Roberts TM, Ward S. 42.  1982. Membrane flow during nematode spermiogenesis. J. Cell Biol. 92:113–20 [Google Scholar]
  43. Aguado-Velasco C, Bretscher MS. 43.  1999. Circulation of the plasma membrane in Dictyostelium. Mol. Biol. Cell 10:4419–27 [Google Scholar]
  44. Traynor D, Kay RR. 44.  2007. Possible roles of the endocytic cycle in cell motility. J. Cell Sci. 120:2318–27 [Google Scholar]
  45. Damer CK, O'Halloran TJ. 45.  2000. Spatially regulated recruitment of clathrin to the plasma membrane during capping and cell translocation. Mol. Biol. Cell 11:2151–59 [Google Scholar]
  46. Fey P, Stephens S, Titus MA, Chisholm RL. 46.  2002. SadA, a novel adhesion receptor in Dictyostelium. J. Cell Biol. 159:1109–19 [Google Scholar]
  47. Cornillon S, Gebbie L, Benghezal M, Nair P, Keller S. 47.  et al. 2006. An adhesion molecule in free-living Dictyostelium amoebae with integrin β features. EMBO Rep. 7:617–21 [Google Scholar]
  48. Zaki M, King J, Futterer K, Insall RH. 48.  2007. Replacement of the essential Dictyostelium Arp2 gene by its Entamoeba homologue using parasexual genetics. BMC Genet. 8:28 [Google Scholar]
  49. Langridge PD, Kay RR. 49.  2007. Mutants in the Dictyostelium Arp2/3 complex and chemoattractant-induced actin polymerization. Exp. Cell Res. 313:2563–74 [Google Scholar]
  50. De Lozanne A, Spudich JA. 50.  1987. Disruption of the Dictyostelium myosin heavy chain gene by homologous recombination. Science 236:1086–91 [Google Scholar]
  51. Witke W, Schleicher M, Noegel AA. 51.  1992. Redundancy in the microfilament system: abnormal development of Dictyostelium cells lacking two F-actin cross-linking proteins. Cell 68:53–62 [Google Scholar]
  52. Shu S, Liu X, Kriebel PW, Daniels MP, Korn ED. 52.  2012. Actin cross-linking proteins cortexillin I and II are required for cAMP signaling during Dictyostelium chemotaxis and development. Mol. Biol. Cell 23:390–400 [Google Scholar]
  53. Noegel AA, Schleicher M. 53.  2000. The actin cytoskeleton of Dictyostelium: a story told by mutants. J. Cell Sci. 113:759–66 [Google Scholar]
  54. Niswonger ML, O'Halloran TJ. 54.  1997. Clathrin heavy chain is required for spore cell but not stalk cell differentiation in Dictyostelium discoideum. Development 124:443–51 [Google Scholar]
  55. Thompson CR, Bretscher MS. 55.  2002. Cell polarity and locomotion, as well as endocytosis, depend on NSF. Development 129:4185–92 [Google Scholar]
  56. Bretscher MS, Clotworthy M. 56.  2007. Using single loxP sites to enhance homologous recombination: ts mutants in Sec1 of Dictyostelium discoideum. PLoS ONE 2:e724 [Google Scholar]
  57. Zanchi R, Howard G, Bretscher MS, Kay RR. 57.  2010. The exocytic gene secA is required for Dictyostelium cell motility and osmoregulation. J. Cell Sci. 123:3226–34 [Google Scholar]
  58. Sollner T, Whiteheart SW, Brunner M, Erdjument-Bromage H, Geromanos S. 58.  et al. 1993. SNAP receptors implicated in vesicle targeting and fusion. Nature 362:318–24 [Google Scholar]
  59. Grote E, Carr CM, Novick PJ. 59.  2000. Ordering the final events in yeast exocytosis. J. Cell Biol. 151:439–52 [Google Scholar]
  60. Kay RR, Langridge P, Traynor D, Hoeller O. 60.  2008. Changing directions in the study of chemotaxis. Nat. Rev. Mol. Cell Biol. 9:455–63 [Google Scholar]
  61. Howe JD, Barry NP, Bretscher MS. 61.  2013. How do amoebae swim and crawl?. PLoS ONE 8:e74382 [Google Scholar]
  62. Ueda M, Sako Y, Tanaka T, Devreotes P, Yanagida T. 62.  2001. Single-molecule analysis of chemotactic signaling in Dictyostelium cells. Science 294:864–67 [Google Scholar]
  63. Xiao Z, Zhang N, Murphy DB, Devreotes PN. 63.  1997. Dynamic distribution of chemoattractant receptors in living cells during chemotaxis and persistent stimulation. J. Cell Biol. 139:365–74 [Google Scholar]
  64. Bretscher MS.64.  1996. Expression and changing distribution of the human transferrin receptor in developing Drosophila oocytes and embryos. J. Cell Sci. 109:3113–19 [Google Scholar]
  65. Kemphues KR, Priess JR, Morton DG, Cheng NS. 65.  1988. Identification of genes required for cytoplasmic localization in early C. elegans embryos. Cell 52:311–20 [Google Scholar]
  66. Hird SN, White JG. 66.  1993. Cortical and cytoplasmic flow polarity in early embryonic cells of Caenorhabditis elegans. J. Cell Biol. 121:1343–55 [Google Scholar]
  67. Wallenfang MR, Seydoux G. 67.  2000. Polarization of the anterior-posterior axis of C. elegans is a microtubule-directed process. Nature 408:89–92 [Google Scholar]
  68. Munro E, Nance J, Priess JR. 68.  2004. Cortical flows powered by asymmetrical contraction transport PAR proteins to establish and maintain anterior-posterior polarity in the early C. elegans embryo. Dev. Cell 7:413–24 [Google Scholar]
  69. Nakayama Y, Shivas JM, Poole DS, Squirrell JM, Kulkoski JM. 69.  et al. 2009. Dynamin participates in the maintenance of anterior polarity in the Caenorhabditis elegans embryo. Dev. Cell 16:889–900 [Google Scholar]
  70. Goehring NW, Trong PK, Bois JS, Chowdhury D, Nicola EM. 70.  et al. 2011. Polarization of PAR proteins by advective triggering of a pattern-forming system. Science 334:1137–41 [Google Scholar]
  71. Balklava Z, Pant S, Fares H, Grant BD. 71.  2007. Genome-wide analysis identifies a general requirement for polarity proteins in endocytic traffic. Nat. Cell Biol. 9:1066–73 [Google Scholar]
  72. Goehring NW, Hoege C, Grill SW, Hyman AA. 72.  2011. PAR proteins diffuse freely across the anterior-posterior boundary in polarized C. elegans embryos. J. Cell Biol. 193:583–94 [Google Scholar]
  73. Tostevin F, Howard M. 73.  2008. Modeling the establishment of PAR protein polarity in the one-cell C. elegans embryo. Biophys. J. 95:4512–22 [Google Scholar]
  74. Cushman SW, Wardzala LJ. 74.  1980. Potential mechanism of insulin action on glucose transport in the isolated rat adipose cell. Apparent translocation of intracellular transport systems to the plasma membrane. J. Biol. Chem. 255:4758–62 [Google Scholar]
  75. Suzuki K, Kono T. 75.  1980. Evidence that insulin causes translocation of glucose transport activity to the plasma membrane from an intracellular storage site. Proc. Natl. Acad. Sci. USA 77:2542–45 [Google Scholar]
  76. Zonies S, Motegi F, Hao Y, Seydoux G. 76.  2010. Symmetry breaking and polarization of the C. elegans zygote by the polarity protein PAR-2. Development 137:1669–77 [Google Scholar]
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