Water permeation drives tumor cell migration in confined microenvironments

Cell

Volumn 157, Issue 3, 2014, Pages 611-623

  Stroka, Kimberly M ^a,b   Jiang, Hongyuan ^a,d   Chen, Shih Hsun ^a   Tong, Ziqiu ^a,b   Wirtz, Denis ^a,b   Sun, Sean X ^a,b,c   Konstantopoulos, Konstantinos ^a,b,c  

^a Johns Hopkins University   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c Johns Hopkins University   (United States)

^d UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; AQUAPORIN; MYOSIN II; SMALL INTERFERING RNA; WATER;

ACTIN POLYMERIZATION; ARTICLE; BREAST CANCER; CANCER CELL; CELL MEMBRANE PERMEABILITY; CELL MIGRATION; CELL VOLUME; CONTROLLED STUDY; HUMAN; HUMAN CELL; MATHEMATICAL MODEL; MICROENVIRONMENT; OSMOTIC STRESS; PRIORITY JOURNAL; TUMOR CELL;

ACTINS; ANIMALS; AQUAPORIN 5; CELL LINE, TUMOR; CELL MEMBRANE; CELL MOVEMENT; CELL SIZE; HUMANS; MICE; MODELS, BIOLOGICAL; SODIUM-HYDROGEN ANTIPORTER; WATER;

EID: 84899623190     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.02.052     Document Type: Article

References (62)

1. S. Alexander, G.E. Koehl, M. Hirschberg, E.K. Geissler, and P. Friedl Dynamic imaging of cancer growth and invasion: a modified skin-fold chamber model Histochem. Cell Biol. 130 2008 1147 1154
2. P.J. Atzberger, S. Isaacson, and C.S. Peskin A microfluidic pumping mechanism driven by non-equilibrium osmotic effects Physica D 238 2009 1168 1179
3. E.M. Balzer, Z. Tong, C.D. Paul, W.C. Hung, K.M. Stroka, A.E. Boggs, S.S. Martin, and K. Konstantopoulos Physical confinement alters tumor cell adhesion and migration phenotypes FASEB J. 26 2012 4045 4056
4. A.R. Beltran, M.A. Ramirez, L.R. Carraro-Lacroix, Y. Hiraki, N.A. Reboucas, and G. Malnic NHE1, NHE2, and NHE4 contribute to regulation of cell pH in T84 colon cancer cells Pflugers Arch. 455 2008 799 810
5. Y.K. Chae, J. Woo, M.J. Kim, S.K. Kang, M.S. Kim, J. Lee, S.K. Lee, G. Gong, Y.H. Kim, and J.C. Soria et al. Expression of aquaporin 5 (AQP5) promotes tumor invasion in human non small cell lung cancer PLoS ONE 3 2008 e2162
6. G.T. Charras, J.C. Yarrow, M.A. Horton, L. Mahadevan, and T.J. Mitchison Non-equilibration of hydrostatic pressure in blebbing cells Nature 435 2005 365 369
7. H.J. Chung, Y.N. Jan, and L.Y. Jan Polarized axonal surface expression of neuronal KCNQ channels is mediated by multiple signals in the KCNQ2 and KCNQ3 C-terminal domains Proc. Natl. Acad. Sci. USA 103 2006 8870 8875
8. V. Dreval, P. Dieterich, C. Stock, and A. Schwab The role of Ca2+ transport across the plasma membrane for cell migration Cell. Physiol. Biochem. 16 2005 119 126
9. P. Friedl, and S. Alexander Cancer invasion and the microenvironment: plasticity and reciprocity Cell 147 2011 992 1009
10. G.G. Goss, M. Woodside, S. Wakabayashi, J. Pouyssegur, T. Waddell, G.P. Downey, and S. Grinstein ATP dependence of NHE-1, the ubiquitous isoform of the Na+/H+ antiporter. Analysis of phosphorylation and subcellular localization J. Biol. Chem. 269 1994 8741 8748
11. S. Grinstein, M. Woodside, T.K. Waddell, G.P. Downey, J. Orlowski, J. Pouyssegur, D.C. Wong, and J.K. Foskett Focal localization of the NHE-1 isoform of the Na+/H+ antiport: assessment of effects on intracellular pH EMBO J. 12 1993 5209 5218
12. M. Grunnet, N. MacAulay, N.K. Jorgensen, S. Jensen, S.P. Olesen, and D.A. Klaerke Regulation of cloned, Ca2+-activated K+ channels by cell volume changes Pflugers Arch. 444 2002 167 177
13. W.C. Hung, S.H. Chen, C.D. Paul, K.M. Stroka, Y.C. Lo, J.T. Yang, and K. Konstantopoulos Distinct signaling mechanisms regulate migration in unconfined versus confined spaces J. Cell Biol. 202 2013 807 824
14. T. Iwasaki, and Y.L. Wang Cytoplasmic force gradient in migrating adhesive cells Biophys. J. 94 2008 L35 L37
15. M. Jaeger, M. Carin, M. Medale, and G. Tryggvason The osmotic migration of cells in a solute gradient Biophys. J. 77 1999 1257 1267
16. H.Y. Jiang, and S.X. Sun Cellular pressure and volume regulation and implications for cell mechanics Biophys. J. 105 2013 609 619
17. H.J. Jung, J.Y. Park, H.S. Jeon, and T.H. Kwon Aquaporin-5: a marker protein for proliferation and migration of human breast cancer cells PLoS ONE 6 2011 e28492
18. K. Keren, P.T. Yam, A. Kinkhabwala, A. Mogilner, and J.A. Theriot Intracellular fluid flow in rapidly moving cells Nat. Cell Biol. 11 2009 1219 1224
19. M. Klein, P. Seeger, B. Schuricht, S.L. Alper, and A. Schwab Polarization of Na(+)/H(+) and Cl(-)/HCO (3)(-) exchangers in migrating renal epithelial cells J. Gen. Physiol. 115 2000 599 608
20. K. Konstantopoulos, P.-H. Wu, and D. Wirtz Dimensional control of cancer cell migration Biophys. J. 104 2013 279 280
21. F. Lang, G.L. Busch, M. Ritter, H. Völkl, S. Waldegger, E. Gulbins, and D. Häussinger Functional significance of cell volume regulatory mechanisms Physiol. Rev. 78 1998 247 306
22. C. Mazzochi, J.K. Bubien, P.R. Smith, and D.J. Benos The carboxyl terminus of the alpha-subunit of the amiloride-sensitive epithelial sodium channel binds to F-actin J. Biol. Chem. 281 2006 6528 6538
23. L.A. Mingle, N.N. Okuhama, J. Shi, R.H. Singer, J. Condeelis, and G. Liu Localization of all seven messenger RNAs for the actin-polymerization nucleator Arp2/3 complex in the protrusions of fibroblasts J. Cell Sci. 118 2005 2425 2433
24. T.J. Mitchison, G.T. Charras, and L. Mahadevan Implications of a poroelastic cytoplasm for the dynamics of animal cell shape Semin. Cell Dev. Biol. 19 2008 215 223
25. A. Mogilner, and G. Oster Cell motility driven by actin polymerization Biophys. J. 71 1996 3030 3045
26. G.F. Oster, and A.S. Perelson The physics of cell motility J. Cell Sci. Suppl. 8 1987 35 54
27. A. Palamidessi, E. Frittoli, M. Garré, M. Faretta, M. Mione, I. Testa, A. Diaspro, L. Lanzetti, G. Scita, and P.P. Di Fiore Endocytic trafficking of Rac is required for the spatial restriction of signaling in cell migration Cell 134 2008 135 147
28. M.C. Papadopoulos, S. Saadoun, and A.S. Verkman Aquaporins and cell migration Pflugers Arch. 456 2008 693 700
29. A. Pathak, and S. Kumar Independent regulation of tumor cell migration by matrix stiffness and confinement Proc. Natl. Acad. Sci. USA 109 2012 10334 10339
30. T.D. Pollard, and G.G. Borisy Cellular motility driven by assembly and disassembly of actin filaments Cell 112 2003 453 465
31. H.V. Prentice-Mott, C.H. Chang, L. Mahadevan, T.J. Mitchison, D. Irimia, and J.V. Shah Biased migration of confined neutrophil-like cells in asymmetric hydraulic environments Proc. Natl. Acad. Sci. USA 110 2013 21006 21011
32. M. Ritter, P. Schratzberger, H. Rossmann, E. Wöll, K. Seiler, U. Seidler, N. Reinisch, C.M. Kähler, H. Zwierzina, and H.J. Lang et al. Effect of inhibitors of Na+/H+-exchange and gastric H+/K+ ATPase on cell volume, intracellular pH and migration of human polymorphonuclear leucocytes Br. J. Pharmacol. 124 1998 627 638
33. A. Schwab Ion channels and transporters on the move News Physiol. Sci. 16 2001 29 33
34. A. Schwab, V. Nechyporuk-Zloy, A. Fabian, and C. Stock Cells move when ions and water flow Pflugers Arch. 453 2007 421 432
35. A. Schwab, A. Fabian, P.J. Hanley, and C. Stock Role of ion channels and transporters in cell migration Physiol. Rev. 92 2012 1865 1913
36. V.K. Sidhaye, E. Chau, V. Srivastava, S. Sirimalle, C. Balabhadrapatruni, N.R. Aggarwal, F.R. D'Alessio, D.N. Robinson, and L.S. King A novel role for aquaporin-5 in enhancing microtubule organization and stability PLoS ONE 7 2012 e38717
37. S.E. Spagnolie, and E. Lauga Jet propulsion without inertia Phys. Fluids 22 2010 081902
38. M.P. Stewart, J. Helenius, Y. Toyoda, S.P. Ramanathan, D.J. Muller, and A.A. Hyman Hydrostatic pressure and the actomyosin cortex drive mitotic cell rounding Nature 469 2011 226 230
39. K.M. Stroka, H.N. Hayenga, and H. Aranda-Espinoza Human neutrophil cytoskeletal dynamics and contractility actively contribute to trans-endothelial migration PLoS ONE 8 2013 e61377
40. L.A. Taber, Y.F. Shi, L. Yang, and P.V. Bayly A poroelastic model for cell crawling including mechanical coupling between cytoskeletal contraction and actin polymerization J. Mech. Mater. Struct. 6 2011 569 589
41. Z.Q. Tong, E.M. Balzer, M.R. Dallas, W.C. Hung, K.J. Stebe, and K. Konstantopoulos Chemotaxis of cell populations through confined spaces at single-cell resolution PLoS ONE 7 2012 e29211
42. S. Wakabayashi, P. Fafournoux, C. Sardet, and J. Pouysségur The Na+/H+ antiporter cytoplasmic domain mediates growth factor signals and controls "H(+)-sensing" Proc. Natl. Acad. Sci. USA 89 1992 2424 2428
43. F. Wehner, H. Olsen, H. Tinel, E. Kinne-Saffran, and R.K. Kinne Cell volume regulation: osmolytes, osmolyte transport, and signal transduction Rev. Physiol. Biochem. Pharmacol. 148 2003 1 80
44. D. Wirtz, K. Konstantopoulos, and P.C. Searson The physics of cancer: the role of physical interactions and mechanical forces in metastasis Nat. Rev. Cancer 11 2011 512 522
45. K. Wolf, S. Alexander, V. Schacht, L.M. Coussens, U.H. von Andrian, J. van Rheenen, E. Deryugina, and P. Friedl Collagen-based cell migration models in vitro and in vivo Semin. Cell Dev. Biol. 20 2009 931 941
46. S. Yadav, S. Puri, and A.D. Linstedt A primary role for Golgi positioning in directed secretion, cell polarity, and wound healing Mol. Biol. Cell 20 2009 1728 1736
47. E.M. Balzer, Z. Tong, C.D. Paul, W.C. Hung, K.M. Stroka, A.E. Boggs, S.S. Martin, and K. Konstantopoulos Physical confinement alters tumor cell adhesion and migration phenotypes FASEB J. 26 2012 4045 4056
48. H.T. Edzes, and H.J. Berendsen The physical state of diffusible ions in cells Annu. Rev. Biophys. Bioeng. 4 1975 265 285
49. R.J. Hawkins, M. Piel, G. Faure-Andre, A.M. Lennon-Dumenil, J.F. Joanny, J. Prost, and R. Voituriez Pushing off the walls: a mechanism of cell motility in confinement Phys. Rev. Lett. 102 2009 058103
50. W.C. Hung, S.H. Chen, C.D. Paul, K.M. Stroka, Y.C. Lo, J.T. Yang, and K. Konstantopoulos Distinct signaling mechanisms regulate migration in unconfined versus confined spaces J. Cell Biol. 202 2013 807 824
51. D. Irimia, and M. Toner Spontaneous migration of cancer cells under conditions of mechanical confinement Integr. Biol. (Camb.) 1 2009 506 512
52. H.Y. Jiang, and S.X. Sun Cellular pressure and volume regulation and implications for cell mechanics Biophys. J. 105 2013 609 619
53. C. Kung A possible unifying principle for mechanosensation Nature 436 2005 647 654
54. T.G. Kuznetsova, M.N. Starodubtseva, N.I. Yegorenkov, S.A. Chizhik, and R.I. Zhdanov Atomic force microscopy probing of cell elasticity Micron 38 2007 824 833
55. K. Luby-Phelps Cytoarchitecture and physical properties of cytoplasm: volume, viscosity, diffusion, intracellular surface area Int. Rev. Cytol. 192 2000 189 221
56. S.J. Marrink, and H.J.C. Berendsen Simulation of water transport through a lipid-membrane J. Phys. Chem. 98 1994 4155 4168
57. D. Pesen, and J.H. Hoh Micromechanical architecture of the endothelial cell cortex Biophys. J. 88 2005 670 679
58. J.J.H.H.M.d. Pont, and S.L. Bonting Membrane Transport 1981 Elsevier/North-Holland Biomedical Press Amsterdam
59. P.S. Raman, C.D. Paul, K.M. Stroka, and K. Konstantopoulos Probing cell traction forces in confined microenvironments Lab Chip 13 2013 4599 4607
60. S.I. Sukharev, B. Martinac, V.Y. Arshavsky, and C. Kung Two types of mechanosensitive channels in the Escherichia coli cell envelope: solubilization and functional reconstitution Biophys. J. 65 1993 177 183
61. J.Y. Tinevez, U. Schulze, G. Salbreux, J. Roensch, J.F. Joanny, and E. Paluch Role of cortical tension in bleb growth Proc. Natl. Acad. Sci. USA 106 2009 18581 18586
62. Z.Q. Tong, E.M. Balzer, M.R. Dallas, W.C. Hung, K.J. Stebe, and K. Konstantopoulos Chemotaxis of cell populations through confined spaces at single-cell resolution PLoS ONE 7 2012 e29211