Regulation of RhoA activity by adhesion molecules and mechanotransduction

Current Molecular Medicine

Volumn 14, Issue 2, 2014, Pages 199-208

  Marjoram, R J ^a   Lessey, E C ^a   Burridge, K ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Actin; Adhesion; Cytoskeleton; Force; GTPase; Mechanotransduction; RhoA

Indexed keywords

BETA1 INTEGRIN; CADHERIN; CD18 ANTIGEN; CD31 ANTIGEN; CELL ADHESION MOLECULE; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; IMMUNOGLOBULIN; INTERCELLULAR ADHESION MOLECULE 1; JUNCTIONAL ADHESION MOLECULE A; NECTIN 1; NECTIN 2; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; VASCULOTROPIN RECEPTOR 2;

ARTICLE; CELL ADHESION; CELL CYCLE PHASE; CELL FUNCTION; CELL PROLIFERATION; CELLULAR STRESS RESPONSE; DEPRESSION; EPITHELIUM CELL; GENE EXPRESSION; HUMAN; INFLAMMATION; LEUKOCYTE; MECHANOTRANSDUCTION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SHEAR STRESS; SIGNAL TRANSDUCTION;

ANIMALS; CELL ADHESION; CYTOSKELETON; HUMANS; MECHANOTRANSDUCTION, CELLULAR; RHOA GTP-BINDING PROTEIN;

EID: 84896699258     PISSN: 15665240     EISSN: 18755666     Source Type: Journal    
DOI: 10.2174/1566524014666140128104541     Document Type: Article

References (124)

1. Hoffman BD, Grashoff C, Schwartz MA. Dynamic Molecular Processes Mediate Cellular Mechanotransduction. Nature 2011; 475(7356): 316-23.
2. DuFort CC, Paszek MJ, Weaver VM. Balancing Forces: Architectural Control of Mechanotransduction. Nat Rev Mol Cell Biol 2011; 12(5): 308-19.
3. Hynes RO, Zhao Q. The Evolution of Cell Adhesion. J Cell Biol 2000; 150(2): F89-96.
4. Ingber DE. Cellular Mechanotransduction: Putting All the Pieces Together Again. FASEB J 2006; 20(7): 811-27.
5. Hynes RO. Integrins: Bidirectional, Allosteric Signaling Machines. Cell 2002; 110(6): 673-87.
6. Oda H, Takeichi M. Evolution: Structural and Functional Diversity of Cadherin at the Adherens Junction. J Cell Biol 2011; 193(7): 1137-46.
7. Lessey EC, Guilluy C, Burridge K. From Mechanical Force to Rhoa Activation. Biochemistry 2012; 51(38): 7420-32.
8. Eyckmans J, Boudou T, Yu X, Chen CS. A Hitchhiker's Guide to Mechanobiology. Dev Cell 2011; 21(1): 35-47.
9. Orr AW, Helmke BP, Blackman BR, Schwartz MA. Mechanisms of Mechanotransduction. Dev Cell 2006; 10(1): 11-20.
10. Petrie RJ, Doyle AD, Yamada KM. Random Versus Directionally Persistent Cell Migration. Nat Rev Mol Cell Biol 2009; 10(8): 538-49.
11. Trepat X, Fredberg JJ. Plithotaxis and Emergent Dynamics in Collective Cellular Migration. Trends Cell Biol 2011; 21(11): 638-46.
12. Wozniak MA, Chen CS. Mechanotransduction in Development: A Growing Role for Contractility. Nat Rev Mol Cell Biol 2009; 10(1): 34-43.
13. Stroka KM, Aranda-Espinoza H. A Biophysical View of the Interplay between Mechanical Forces and Signaling Pathways During Transendothelial Cell Migration. FEBS J 2010; 277(5): 1145-58.
14. Ridley AJ, Schwartz MA, Burridge K, et al. Cell Migration: Integrating Signals from Front to Back. Science 2003; 302(5651): 1704-9.
15. Heasman SJ, Ridley AJ. Multiple Roles for Rhoa During T Cell Transendothelial Migration. Small GTPases 2010; 1(3): 174-79.
16. Tambe DT, Hardin CC, Angelini TE, et al. Collective Cell Guidance by Cooperative Intercellular Forces. Nat Mater 2011; 10(6): 469-75.
17. Theveneau E, Marchant L, Kuriyama S, et al. Collective Chemotaxis Requires Contact-Dependent Cell Polarity. Dev Cell 2010; 19(1): 39-53.
18. Montell DJ, Yoon WH, Starz-Gaiano M. Group Choreography: Mechanisms Orchestrating the Collective Movement of Border Cells. Nat Rev Mol Cell Biol 2012; 13(10): 631-45.
19. Friedl P, Gilmour D. Collective Cell Migration in Morphogenesis, Regeneration and Cancer. Nat Rev Mol Cell Biol 2009; 10(7): 445-57.
20. Gorfinkiel N, Blanchard GB. Dynamics of Actomyosin Contractile Activity During Epithelial Morphogenesis. Curr Opin Cell Biol 2011; 23(5): 531-9.
21. He L, Wang X, Tang HL, Montell DJ. Tissue Elongation Requires Oscillating Contractions of a Basal Actomyosin Network. Nat Cell Biol 2010; 12(12): 1133-42.
22. Montell DJ. Morphogenetic Cell Movements: Diversity from Modular Mechanical Properties. Science 2008; 322(5907): 1502-5.
23. Behrndt M, Salbreux G, Campinho P, et al. Forces Driving Epithelial Spreading in Zebrafish Gastrulation. Science 2012; 338(6104): 257-60.
24. Papusheva E, Heisenberg CP. Spatial Organization of Adhesion: Force-Dependent Regulation and Function in Tissue Morphogenesis. EMBO J 2010; 29(16): 2753-68.
25. Murphy AM, Montell DJ. Cell Type-Specific Roles for Cdc42, Rac, and Rhol in Drosophila Oogenesis. J Cell Biol 1996; 133(3): 617-30.
26. Nesbitt WS, Mangin P, Salem HH, Jackson SP. The Impact of Blood Rheology on the Molecular and Cellular Events Underlying Arterial Thrombosis. J Mol Med 2006; 84(12): 989-95.
27. Jackson SP, Nesbitt WS, Westein E. Dynamics of Platelet Thrombus Formation. J Thromb Haemost 2009; 7 (Suppl 1): 17-20.
28. Hahn C, Schwartz MA. Mechanotransduction in Vascular Physiology and Atherogenesis. Nat Rev Mol Cell Biol 2009; 10(1): 53-62.
29. Huynh J, Nishimura N, Rana K, et al. Age-Related Intimal Stiffening Enhances Endothelial Permeability and Leukocyte Transmigration. Sci Transl Med 2011; 3(112): 112ra22.
30. Lusis AJ. Atherosclerosis. Nature 2000; 407(6801): 233-41.
31. Butcher DT, Alliston T, Weaver VM. A Tense Situation: Forcing Tumour Progression. Nat Rev Cancer 2009; 9(2): 108-22.
32. Lu P, Weaver VM, Werb Z. The Extracellular Matrix: A Dynamic Niche in Cancer Progression. J Cell Biol 2012; 196(4): 395-406.
33. Provenzano PP, Inman DR, Eliceiri KW, et al. Collagen Density Promotes Mammary Tumor Initiation and Progression. BMC Med 2008; 6: 11.
34. Paszek MJ, Zahir N, Johnson KR, et al. Tensional Homeostasis and the Malignant Phenotype. Cancer Cell 2005; 8(3): 241-54.
35. Pathak A, Kumar S. Independent Regulation of Tumor Cell Migration by Matrix Stiffness and Confinement. Proc Natl Acad Sci U S A 2012; 109(26): 10334-9.
36. Ulrich TA, Jain A, Tanner K, MacKay JL, Kumar S. Probing Cellular Mechanobiology in Three-Dimensional Culture with Collagen-Agarose Matrices. Biomaterials 2010; 31(7): 1875-84.
37. Zaman MH, Trapani LM, Sieminski AL, et al. Migration of Tumor Cells in 3d Matrices Is Governed by Matrix Stiffness Along with Cell-Matrix Adhesion and Proteolysis. Proc Natl Acad Sci U S A 2006; 103(29): 10889-94.
38. Wennerberg K, Rossman KL, Der CJ. The Ras Superfamily at a Glance. J Cell Sci 2005; 118(Pt 5): 843-6.
39. Jaffe AB, Hall A. Rho Gtpases: Biochemistry and Biology. Annu Rev Cell Dev Biol 2005; 21: 247-69.
40. Garcia-Mata R, Boulter E, Burridge K. The 'Invisible Hand': Regulation of Rho Gtpases by Rhogdis. Nat Rev Mol Cell Biol 2011; 12(8): 493-504.
41. Etienne-Manneville S, Hall A. Rho Gtpases in Cell Biology. Nature 2002; 420(6916): 629-35.
42. Chrzanowska-Wodnicka M, Burridge K. Rho-Stimulated Contractility Drives the Formation of Stress Fibers and Focal Adhesions. J Cell Biol 1996; 133(6): 1403-15.
43. Amano M, Ito M, Kimura K, et al. Phosphorylation and Activation of Myosin by Rho-Associated Kinase (Rho-Kinase). J Biol Chem 1996; 271(34): 20246-9.
44. Kimura K, Ito M, Amano M, et al. Regulation of Myosin Phosphatase by Rho and Rho-Associated Kinase (Rho-Kinase). Science 1996; 273(5272): 245-8.
45. Watanabe N, Madaule P, Reid T, et al. P140mdia, a Mammalian Homolog of Drosophila Diaphanous, Is a Target Protein for Rho Small Gtpase and Is a Ligand for Profilin. EMBO J 1997; 16(11): 3044-56.
46. Maekawa M, Ishizaki T, Boku S, et al. Signaling from Rho to the Actin Cytoskeleton through Protein Kinases Rock and Lim-Kinase. Science 1999; 285(5429): 895-8.
47. Chen CS. Mechanotransduction - a Field Pulling Together? J Cell Sci 2008; 121(Pt 20): 3285-92.
48. Pines M, Das R, Ellis SJ, et al. Mechanical Force Regulates Integrin Turnover in Drosophila in Vivo. Nat Cell Biol 2012; 14(9): 935-43.
49. Heisenberg CP, Bellaiche Y. Forces in Tissue Morphogenesis and Patterning. Cell 2013; 153(5): 948-62.
50. Mammoto T, Ingber DE. Mechanical Control of Tissue and Organ Development. Development 2010; 137(9): 1407-20.
51. Campbell ID, Humphries MJ. Integrin Structure, Activation, and Interactions. Cold Spring Harb Perspect Biol 2011; 3(3).
52. Springer TA, Dustin ML. Integrin inside-out Signaling and the Immunological Synapse. Curr Opin Cell Biol 2012; 24(1): 107-15.
53. Luo BH, Springer TA. Integrin Structures and Conformational Signaling. Curr Opin Cell Biol 2006; 18(5): 579-86.
54. Burridge K, Chrzanowska-Wodnicka M. Focal Adhesions, Contractility, and Signaling. Annu Rev Cell Dev Biol 1996; 12: 463-518.
55. Tamkun JW, DeSimone DW, Fonda D, et al. Structure of Integrin, a Glycoprotein Involved in the Transmembrane Linkage between Fibronectin and Actin. Cell 1986; 46(2): 271-82.
56. Friedland JC, Lee MH, Boettiger D. Mechanically Activated Integrin Switch Controls Alpha5beta1 Function. Science 2009; 323(5914): 642-4.
57. Zhu J, Luo BH, Xiao T, et al. Structure of a Complete Integrin Ectodomain in a Physiologic Resting State and Activation and Deactivation by Applied Forces. Mol Cell 2008; 32(6): 849-61.
58. Jannat RA, Dembo M, Hammer DA. Traction Forces of Neutrophils Migrating on Compliant Substrates. Biophys J 2011; 101(3): 575-84.
59. Lin GL, Cohen DM, Desai RA, et al. Activation of Beta 1 but Not Beta 3 Integrin Increases Cell Traction Forces. FEBS Lett 2013; 587(6): 763-9.
60. Rabinovitz I, Gipson IK, Mercurio AM. Traction Forces Mediated by Alpha6beta4 Integrin: Implications for Basement Membrane Organization and Tumor Invasion. Mol Biol Cell 2001; 12(12): 4030-43.
61. Svitkina TM, Verkhovsky AB, McQuade KM, Borisy GG. Analysis of the Actin-Myosin Ii System in Fish Epidermal Keratocytes: Mechanism of Cell Body Translocation. J Cell Biol 1997; 139(2): 397-415.
62. von Wichert G, Haimovich B, Feng GS, Sheetz MP. Force-Dependent Integrin-Cytoskeleton Linkage Formation Requires Downregulation of Focal Complex Dynamics by Shp2. EMBO J 2003; 22(19): 5023-35.
63. Galbraith CG, Sheetz MP. Keratocytes Pull with Similar Forces on Their Dorsal and Ventral Surfaces. J Cell Biol 1999; 147(6): 1313-24.
64. Plotnikov SV, Pasapera AM, Sabass B, Waterman CM. Force Fluctuations within Focal Adhesions Mediate Ecm-Rigidity Sensing to Guide Directed Cell Migration. Cell 2012; 151(7): 1513-27.
65. Ren XD, Kiosses WB, Schwartz MA. Regulation of the Small Gtp-Binding Protein Rho by Cell Adhesion and the Cytoskeleton. EMBO J 1999; 18(3): 578-85.
66. Arthur WT, Petch LA, Burridge K. Integrin Engagement Suppresses Rhoa Activity Via a C-Src-Dependent Mechanism. Curr Biol 2000; 10(12): 719-22.
67. Bradley WD, Hernandez SE, Settleman J, Koleske AJ. Integrin Signaling through Arg Activates P190rhogap by Promoting Its Binding to P120rasgap and Recruitment to the Membrane. Mol Biol Cell 2006; 17(11): 4827-36.
68. Arthur WT, Burridge K. Rhoa Inactivation by P190rhogap Regulates Cell Spreading and Migration by Promoting Membrane Protrusion and Polarity. Mol Biol Cell 2001; 12(9): 2711-20.
69. Dubash AD, Wennerberg K, Garcia-Mata R, et al. A Novel Role for Lsc/P115 Rhogef and Larg in Regulating Rhoa Activity Downstream of Adhesion to Fibronectin. J Cell Sci 2007; 120(Pt 22): 3989-98.
70. Lim Y, Lim ST, Tomar A, et al. Pyk2 and Fak Connections to P190rho Guanine Nucleotide Exchange Factor Regulate Rhoa Activity, Focal Adhesion Formation, and Cell Motility. J Cell Biol 2008; 180(1): 187-203.
71. Tomar A, Lim ST, Lim Y, Schlaepfer DD. A Fak-P120rasgap-P190rhogap Complex Regulates Polarity in Migrating Cells. J Cell Sci 2009; 122(Pt 11): 1852-62.
72. Wang N, Butler JP, Ingber DE. Mechanotransduction across the Cell Surface and through the Cytoskeleton. Science 1993; 260(5111): 1124-7.
73. Choquet D, Felsenfeld DP, Sheetz MP. Extracellular Matrix Rigidity Causes Strengthening of Integrin-Cytoskeleton Linkages. Cell 1997; 88(1): 39-48.
74. Matthews BD, Overby DR, Mannix R, Ingber DE. Cellular Adaptation to Mechanical Stress: Role of Integrins, Rho, Cytoskeletal Tension and Mechanosensitive Ion Channels. J Cell Sci 2006; 119(Pt 3): 508-18.
75. Feral CC, Zijlstra A, Tkachenko E, et al. Cd98hc (Slc3a2) Participates in Fibronectin Matrix Assembly by Mediating Integrin Signaling. J Cell Biol 2007; 178(4): 701-11.
76. Boulter E, Estrach S, Errante A, et al. Cd98hc (Slc3a2) Regulation of Skin Homeostasis Wanes with Age. J Exp Med 2013; 210(1): 173-90.
77. Guilluy C, Swaminathan V, Garcia-Mata R, et al. The Rho Gefs Larg and Gef-H1 Regulate the Mechanical Response to Force on Integrins. Nat Cell Biol 2011; 13(6): 722-7.
78. Brieher WM, Yap AS. Cadherin Junctions and Their Cytoskeleton(S). Curr Opin Cell Biol 2013; 25(1): 39-46.
79. Sahai E, Marshall CJ. Rock and Dia Have Opposing Effects on Adherens Junctions Downstream of Rho. Nat Cell Biol 2002; 4(6): 408-15.
80. Ngok SP, Geyer R, Liu M, et al. Vegf and Angiopoietin-1 Exert Opposing Effects on Cell Junctions by Regulating the Rho Gef Syx. J Cell Biol 2012; 199(7): 1103-15.
81. Allport JR, Ding H, Collins T, Gerritsen ME, Luscinskas FW. Endothelial-Dependent Mechanisms Regulate Leukocyte Transmigration: A Process Involving the Proteasome and Disruption of the Vascular Endothelial-Cadherin Complex at Endothelial Cell-to-Cell Junctions. J Exp Med 1997; 186(4): 517-27.
82. Moll T, Dejana E, Vestweber D. In Vitro Degradation of Endothelial Catenins by a Neutrophil Protease. J Cell Biol 1998; 140(2): 403-7.
83. Citi S. Protein Kinase Inhibitors Prevent Junction Dissociation Induced by Low Extracellular Calcium in Mdck Epithelial Cells. J Cell Biol 1992; 117(1): 169-78.
84. Citi S, Volberg T, Bershadsky AD, Denisenko N, Geiger B. Cytoskeletal Involvement in the Modulation of Cell-Cell Junctions by the Protein Kinase Inhibitor H-7. J Cell Sci 1994; 107(Pt 3): 683-92.
85. Uehata M, Ishizaki T, Satoh H, et al. Calcium Sensitization of Smooth Muscle Mediated by a Rho-Associated Protein Kinase in Hypertension. Nature 1997; 389(6654): 990-4.
86. Gomez GA, McLachlan RW, Yap AS. Productive Tension: Force-Sensing and Homeostasis of Cell-Cell Junctions. Trends Cell Biol 2011; 21(9): 499-505.
87. Yonemura S, Wada Y, Watanabe T, Nagafuchi A, Shibata M. Alpha-Catenin as a Tension Transducer That Induces Adherens Junction Development. Nat Cell Biol 2010; 12(6): 533-42.
88. le Duc Q, Shi Q, Blonk I, et al. Vinculin Potentiates E-Cadherin Mechanosensing and Is Recruited to Actin-Anchored Sites within Adherens Junctions in a Myosin Ii-Dependent Manner. J Cell Biol 2010; 189(7): 1107-15.
89. Borghi N, Sorokina M, Shcherbakova OG, et al. E-Cadherin Is under Constitutive Actomyosin-Generated Tension That Is Increased at Cell-Cell Contacts Upon Externally Applied Stretch. Proc Natl Acad Sci U S A 2012; 109(31): 12568-73.
90. Noren NK, Niessen CM, Gumbiner BM, Burridge K. Cadherin Engagement Regulates Rho Family Gtpases. J Biol Chem 2001; 276(36): 33305-8.
91. Lampugnani MG, Zanetti A, Breviario F, et al. Ve-Cadherin Regulates Endothelial Actin Activating Rac and Increasing Membrane Association of Tiam. Mol Biol Cell 2002; 13(4): 1175-89.
92. Noren NK, Arthur WT, Burridge K. Cadherin Engagement Inhibits Rhoa Via P190rhogap. J Biol Chem 2003; 278(16): 13615-8.
93. Omelchenko T, Hall A. Myosin-Ixa Regulates Collective Epithelial Cell Migration by Targeting Rhogap Activity to Cell-Cell Junctions. Curr Biol 2012; 22(4): 278-88.
94. Calautti E, Grossi M, Mammucari C, et al. Fyn Tyrosine Kinase Is a Downstream Mediator of Rho/Prk2 Function in Keratinocyte Cell-Cell Adhesion. J Cell Biol 2002; 156(1): 137-48.
95. Nelson CM, Pirone DM, Tan JL, Chen CS. Vascular Endothelial-Cadherin Regulates Cytoskeletal Tension, Cell Spreading, and Focal Adhesions by Stimulating Rhoa. Mol Biol Cell 2004; 15(6): 2943-53.
96. Charrasse S, Meriane M, Comunale F, Blangy A, Gauthier-Rouviere C. N-Cadherin-Dependent Cell-Cell Contact Regulates Rho Gtpases and Beta-Catenin Localization in Mouse C2c12 Myoblasts. J Cell Biol 2002; 158(5): 953-65.
97. Newman PJ. The Biology of Pecam-1. J Clin Invest 1997; 99(1): 3-8.
98. Privratsky JR, Newman DK, Newman PJ. Pecam-1: Conflicts of Interest in Inflammation. Life Sci 2010; 87(3-4): 69-82.
99. Muller WA, Weigl SA, Deng X, Phillips DM. Pecam-1 Is Required for Transendothelial Migration of Leukocytes. J Exp Med 1993; 178(2): 449-60.
100. Woodfin A, Voisin MB, Imhof BA, et al. Endothelial Cell Activation Leads to Neutrophil Transmigration as Supported by the Sequential Roles of Icam-2, Jam-a, and Pecam-1. Blood 2009; 113(24): 6246-57.
101. Muller WA, Ratti CM, McDonnell SL, Cohn ZA. A Human Endothelial Cell-Restricted, Externally Disposed Plasmalemmal Protein Enriched in Intercellular Junctions. J Exp Med 1989; 170(2): 399-414.
102. Albelda SM, Oliver PD, Romer LH, Buck CA. Endocam: A Novel Endothelial Cell-Cell Adhesion Molecule. J Cell Biol 1990; 110(4): 1227-37.
103. Osawa M, Masuda M, Harada N, Lopes RB, Fujiwara K. Tyrosine Phosphorylation of Platelet Endothelial Cell Adhesion Molecule-1 (Pecam-1, Cd31) in Mechanically Stimulated Vascular Endothelial Cells. Eur J Cell Biol 1997; 72(3): 229-37.
104. Osawa M, Masuda M, Kusano K, Fujiwara K. Evidence for a Role of Platelet Endothelial Cell Adhesion Molecule-1 in Endothelial Cell Mechanosignal Transduction: Is It a Mechanoresponsive Molecule? J Cell Biol 2002; 158(4): 773-85.
105. Tzima E, Irani-Tehrani M, Kiosses WB, et al. A Mechanosensory Complex That Mediates the Endothelial Cell Response to Fluid Shear Stress. Nature 2005; 437(7057): 426-31.
106. Chiu YJ, McBeath E, Fujiwara K. Mechanotransduction in an Extracted Cell Model: Fyn Drives Stretch- and Flow-Elicited Pecam-1 Phosphorylation. J Cell Biol 2008; 182(4): 753-63.
107. Collins C, Guilluy C, Welch C, et al. Localized Tensional Forces on Pecam-1 Elicit a Global Mechanotransduction Response Via the Integrin-Rhoa Pathway. Curr Biol 2012; 22(22): 2087-94.
108. Conway DE, Breckenridge MT, Hinde E, et al. Fluid Shear Stress on Endothelial Cells Modulates Mechanical Tension across Ve-Cadherin and Pecam-1. Curr Biol 2013; 23(11): 1024-30.
109. van de Stolpe A, van der Saag PT. Intercellular Adhesion Molecule-1. J Mol Med (Berl) 1996; 74(1): 13-33.
110. Wittchen ES. Endothelial Signaling in Paracellular and Transcellular Leukocyte Transmigration. Front Biosci 2009; 14: 2522-45.
111. Muller WA. Mechanisms of Leukocyte Transendothelial Migration. Annu Rev Pathol 2011; 6: 323-44.
112. van Buul JD, Kanters E, Hordijk PL. Endothelial Signaling by Ig-Like Cell Adhesion Molecules. Arterioscler Thromb Vasc Biol 2007; 27(9): 1870-6.
113. Smith LA, Aranda-Espinoza H, Haun JB, Dembo M, Hammer DA. Neutrophil Traction Stresses Are Concentrated in the Uropod During Migration. Biophys J 2007; 92(7): L58-60.
114. Jannat RA, Robbins GP, Ricart BG, Dembo M, Hammer DA. Neutrophil Adhesion and Chemotaxis Depend on Substrate Mechanics. J Phys Condens Matter 2010; 22(19): 194117.
115. Rabodzey A, Alcaide P, Luscinskas FW, Ladoux B. Mechanical Forces Induced by the Transendothelial Migration of Human Neutrophils. Biophys J 2008; 95(3): 1428-38.
116. Liu Z, Sniadecki NJ, Chen CS. Mechanical Forces in Endothelial Cells During Firm Adhesion and Early Transmigration of Human Monocytes. Cell Mol Bioeng 2010; 3(1): 50-59.
117. Mandell KJ, Parkos CA. The Jam Family of Proteins. Adv Drug Deliv Rev 2005; 57(6): 857-67.
118. Severson EA, Parkos CA. Mechanisms of Outside-in Signaling at the Tight Junction by Junctional Adhesion Molecule A. Ann N Y Acad Sci 2009; 1165: 10-8.
119. Utech M, Ivanov AI, Samarin SN, et al. Mechanism of Ifn-Gamma-Induced Endocytosis of Tight Junction Proteins: Myosin Ii-Dependent Vacuolarization of the Apical Plasma Membrane. Mol Biol Cell 2005; 16(10): 5040-52.
120. Stamatovic SM, Sladojevic N, Keep RF, Andjelkovic AV. Relocalization of Junctional Adhesion Molecule a During Inflammatory Stimulation of Brain Endothelial Cells. Mol Cell Biol 2012; 32(17): 3414-27.
121. Wojcikiewicz EP, Koenen RR, Fraemohs L, et al. Lfa-1 Binding Destabilizes the Jam-a Homophilic Interaction During Leukocyte Transmigration. Biophys J 2009; 96(1): 285-93.
122. Rikitake Y, Mandai K, Takai Y. The Role of Nectins in Different Types of Cell-Cell Adhesion. J Cell Sci 2012; 125(Pt 16): 3713-22.
123. Ikeda W, Nakanishi H, Miyoshi J, et al. Afadin: A Key Molecule Essential for Structural Organization of Cell-Cell Junctions of Polarized Epithelia During Embryogenesis. J Cell Biol 1999; 146(5): 1117-32.
124. Clement C, Tiwari V, Scanlan PM, et al. A Novel Role for Phagocytosis-Like Uptake in Herpes Simplex Virus Entry. J Cell Biol 2006; 174(7): 1009-21.