Integrins and Small GTPases as Modulators of Phagocytosis

International Review of Cell and Molecular Biology

Volumn 302, Issue , 2013, Pages 321-354

  Sayedyahossein, Samar ^a   Dagnino, Lina ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Integrin; Nonprofessional phagocytes; Particle engulfment; Phagocytosis; Rho GTPases

Indexed keywords

ACTIN RELATED PROTEIN 2; ACTIN RELATED PROTEIN 3; BETA5 INTEGRIN; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; F ACTIN; FIBRONECTIN BINDING PROTEIN; FOCAL ADHESION KINASE; GALECTIN 3; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE TRIPHOSPHATASE; INTEGRIN; INTEGRIN LINKED KINASE; INTERCELLULAR ADHESION MOLECULE 3; KERATINOCYTE GROWTH FACTOR; LACTADHERIN; LIPOCORTIN 2; MYOSIN II; MYOSIN VIIA; PAXILLIN; PEROXYNITRITE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN CDC42; PROTEIN KINASE B; PROTEIN TYROSINE KINASE; PROTEINASE ACTIVATED RECEPTOR 2; RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SCAFFOLD PROTEIN; VERY LATE ACTIVATION ANTIGEN 2;

ALZHEIMER DISEASE; APOPTOSIS; ARTICLE; BACTERIAL CELL; CELL ADHESION; CELL INTERACTION; CELL INVASION; CELL MATURATION; CELL MEMBRANE; CELL MIGRATION; DEGENERATIVE DISEASE; ENDOTHELIUM CELL; ENZYME ACTIVATION; EPIDERMIS; EPITHELIUM CELL; EQUINE HERPES VIRUS; HERPES SIMPLEX VIRUS 1; HOMEOSTASIS; HUMAN; HUMAN CYTOMEGALOVIRUS; HUMAN HERPESVIRUS 8; INNATE IMMUNITY; INTERNALIZATION; MECHANOTRANSDUCTION; MESENCHYME CELL; MICROGLIA; MULTIPLE SCLEROSIS; NONHUMAN; PARKINSON DISEASE; PHAGOCYTOSIS; PHAGOSOME; PHOTORECEPTOR; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; RECEPTOR BINDING; RETINA; SIGNAL TRANSDUCTION; VIRUS CELL INTERACTION;

EID: 84872657469     PISSN: 19376448     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-407699-0.00006-6     Document Type: Chapter

References (165)

1. Acconcia F., Barnes C.J., Singh R.R., Talukder A.H., Kumar R. Phosphorylation-dependent regulation of nuclear localization and functions of integrin-linked kinase. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:6782-6787.
2. Agerer F., Lux S., Michel A., Rohde M., Ohlsen K., Hauck C.R. Cellular invasion by Staphylococcus aureus reveals a functional link between focal adhesion kinase and cortactin in integrin-mediated internalisation. J. Cell Sci. 2005, 118:2189-2200.
3. Agerer F., Michel A., Ohlsen K., Hauck C.R. Integrin-mediated invasion of Staphylococcus aureus into human cells requires Src family protein-tyrosine kinases. J. Biol. Chem. 2003, 278:42524-42531.
4. Ait-Oufella H., Pouresmail V., Simon T., Blanc-Brude O., Kinugawa K., Merval R., Offenstadt G., Leseche G., Cohen P.L., Tedgui A., Mallat Z. Defective mer receptor tyrosine kinase signaling in bone marrow cells promotes apoptotic cell accumulation and accelerates atherosclerosis. Arterioscler Thromb. Vasc. Biol. 2008, 28:1429-1431.
5. Akakura S., Singh S., Spataro M., Akakura R., Kim J.L., Albert M.L., Birge R.B. The opsonin MFG-E8 is a ligand for the alphaVbeta5 integrin and triggers DOCK 180-dependent Rac1 activation for the phagocytosis of apoptotic cells. Exp. Cell Res. 2004, 292:403-416.
6. Albert M.L., Kim J.I., Birge R.B. alphavbeta5 integrin recruits the CrkII-Dock180-rac1 complex for phagocytosis of apoptotic cells. Nat. Cell Biol. 2000, 2:899-905.
7. Allen L.A., Aderem A. Molecular definition of distinct cytoskeletal structures involved in complement- and Fc receptor-mediated phagocytosis in macrophages. J. Exp. Med. 1996, 184:627-637.
8. Amelung S., Nerlich A., Rohde M., Spellerberg B., Cole J.N., Nizet V., Chhatwal G.S., Talay S.R. The FbaB-type fibronectin-binding protein of Streptococcus pyogenes promotes specific invasion into endothelial cells. Cell. Microbiol. 2011, 13:1200-1211.
9. Ando H., Niki Y., Ito M., Akiyama K., Matsui M.S., Yarosh D.B., Ichihashi M. Melanosomes are transferred from melanocytes to keratinocytes through the processes of packaging, release, uptake, and dispersion. J. Invest. Dermatol. 2012, 132:1222-1229.
10. Arold S.T. How focal adhesion kinase achieves regulation by linking ligand binding, localization and action. Curr. Opin. Struct. Biol. 2011, 21:808-813.
11. Arora P.D., Conti M.A., Ravid S., Sacks D.B., Kapus A., Adelstein R.S., Bresnick A.R., McCulloch C.A. Rap1 activation in collagen phagocytosis is dependent on nonmuscle myosin II-A. Mol. Biol. Cell 2008, 19:5032-5046.
12. Arora P.D., Marignani P.A., McCulloch C.A. Collagen phagocytosis is regulated by the guanine nucleotide exchange factor Vav2. Am. J. Physiol. Cell Physiol. 2008, 295:C130-C137.
13. Arora P.D., Manolson M.F., Downey G.P., Sodek J., McCulloch C.A. A novel model system for characterization of phagosomal maturation, acidification, and intracellular collagen degradation in fibroblasts. J. Biol. Chem. 2000, 275:35432-35441.
14. Arora P.D., Wang Y., Janmey P.A., Bresnick A., Yin H.L., McCulloch C.A. Gelsolin and non-muscle myosin IIA interact to mediate calcium-regulated collagen phagocytosis. J. Biol. Chem. 2011, 286:34184-34198.
15. Aymeric L., Apetoh L., Ghiringhelli F., Tesniere A., Martins I., Kroemer G., Smyth M.J., Zitvogel L. Tumor cell death and ATP release prime dendritic cells and efficient anticancer immunity. Cancer Res. 2010, 70:855-858.
16. Beller D.I., Springer T.A., Schreiber R.D. Anti-Mac-1 selectively inhibits the mouse and human type three complement receptor. J. Exp. Med. 1982, 156:1000-1009.
17. Belleudi F., Purpura V., Scrofani C., Persechino F., Leone L., Torrisi M.R. Expression and signaling of the tyrosine kinase FGFR2b/KGFR regulates phagocytosis and melanosome uptake in human keratinocytes. FASEB J. 2011, 25:170-181.
18. Bennett M., Yu H., Clarke M. Signalling from dead cells drives inflammation and vessel remodelling. Vasc. Pharmacol. 2012, 56:187-192.
19. Bergelson J.M., Cunningham J.A., Droguett G., Kurt-Jones E.A., Krithivas A., Hong J.S., Horwitz M.S., Crowell R.L., Finberg R.W. Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 1997, 275:1320-1323.
20. Bergmann S., Lang A., Rohde M., Agarwal V., Rennemeier C., Grashoff C., Preissner K.T., Hammerschmidt S. Integrin-linked kinase is required for vitronectin-mediated internalization of Streptococcus pneumoniae by host cells. J. Cell Sci. 2009, 122:256-267.
21. Bhalla S., Shiratsuchi H., Craig D.H., Basson M.D. beta(1)-integrin mediates pressure-stimulated phagocytosis. Am. J. Surg. 2009, 198:611-616.
22. Birkedal-Hansen H., Moore W.G., Bodden M.K., Windsor L.J., Birkedal-Hansen B., DeCarlo A., Engler J.A. Matrix metalloproteinases: a review. Crit. Rev. Oral Biol. Med. 2003, 4:197-250.
23. Block M.L., Zecca L., Hong J.S. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nature reviews. Neuroscience 2007, 8:57-69.
24. Blystone S.D., Graham I.L., Lindberg F.P., Brown E.J. Integrin alpha v beta 3 differentially regulates adhesive and phagocytic functions of the fibronectin receptor alpha 5 beta 1. J. Cell Biol. 1994, 127:1129-1137.
25. Boas F.E., Forman L., Beutler E. Phosphatidylserine exposure and red cell viaility in red cell aging and in hemolytic anemia. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:3077-3081.
26. Boesze-Battaglia K., Albert A.D. Phospholipid distribution among bovine rod outer segment plasma membrane and disk membranes. Exp. Eye Res. 1992, 54:821-823.
27. Bohdanowicz M., Cosio G., Backer J.M., Grinstein S. Class I and class III phosphoinositide 3-kinases are required for actin polymerization that propels phagosomes. J. Cell Biol. 2010, 191:999-1012.
28. Botelho R.J., Grinstein S. Phagocytosis. Curr. Biol. 2011, 21:R533-R538.
29. Brakebusch C., Fassler R. The integrin-actin connection, an eternal love affair. EMBO J. 2003, 22:2324-2333.
30. Braun A., Bordoy R., Stanchi F., Moser M., Kostka G., Ehler E., Fassler R. PINCH2 is a new five LIM domain protein, homologous to PINCH and localized to focal adhesions. Exp. Cell Res. 2003, 284:239-250.
31. Bunting M., Harris E.S., McIntyre T.M., Prescott S.M., Zimmerman G.A. Leukocyte adhesion deficiency syndromes: adhesion and tethering defects involving beta 2 integrins and selectin ligands. Curr. Opin. Hematol. 2002, 9:30-35.
32. Byers H.R., Dykstra S.G., Boissel S.J. Requirement of dynactin p150(Glued) subunit for the functional integrity of the keratinocyte microparasol. J. Invest. Dermatol. 2007, 127:1736-1744.
33. Cardinali G., Bolasco G., Aspite N., Lucania G., Lotti L.V., Torrisi M.R., Picardo M. Melanosome transfer promoted by keratinocyte growth factor in light and dark skin-derived keratinocytes. J. Invest. Dermatol. 2008, 128:558-567.
34. Cardinali G., Ceccarelli S., Kovacs D., Aspite N., Lotti L.V., Torrisi M.R., Picardo M. Keratinocyte growth factor promotes melanosome transfer to keratinocytes. J. Invest. Dermatol. 2005, 125:1190-1199.
35. Caron E., Hall A. Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases. Science 1998, 282:1717-1721.
36. Caron E., Self A.J., Hall A. The GTPase Rap1 controls functional activation of macrophage integrin alphaMbeta2 by LPS and other inflammatory mediators. Curr. Biol. 2000, 10:974-978.
37. Cartwright K. Pneumococcal disease in western Europe: burden of disease, antibiotic resistance and management. Eur. J. Pediatr. 2002, 161:188-195.
38. Chang Y., Finnemann S.C. Tetraspanin CD81 is required for the alphaVbeta5 integrin-dependent particle-binding step of RPE phagocytosis. J. Cell Sci. 2007, 120:3053-3063.
39. Chao M.P., Majeti R., Weissman I.L. Programmed cell removal: a new obstacle in the road to developing cancer. Nat. Rev. Cancer 2012, 12:58-67.
40. Dagnino L. Integrin-linked kinase: a Scaffold protein unique among its ilk. J. Cell Commun. Signal. 2011, 5:81-83.
41. Demali K.A., Jue A.L., Burridge K. IpaA targets beta1 integrins and rho to promote actin cytoskeleton rearrangements necessary for Shigella entry. J. Biol. Chem. 2006, 281:39534-39541.
42. Dery O., Bunnett N.W. Proteinase-activated receptors: a growing family of heptahelical receptors for thrombin, trypsin and tryptase. Biochem. Soc. Trans. 1999, 27:246-254.
43. Deuretzbacher A., Czymmeck N., Reimer R., Trulzsch K., Gaus K., Hohenberg H., Heesemann J., Aepfelbacher M., Ruckdeschel K. Beta1 integrin-dependent engulfment of Yersinia enterocolitica by macrophages is coupled to the activation of autophagy and suppressed by type III protein secretion. J. Immunol. 2009, 183:5847-5860.
44. Dewitt S., Tian W., Hallett M.B. Localised PtdIns(3,4,5)P3 or PtdIns(3,4)P2 at the phagocytic cup is required for both phagosome closure and Ca2+ signalling in HL60 neutrophils. J. Cell Sci. 2006, 119:443-451.
45. Drummond R.A., Brown G.D. The role of Dectin-1 in the host defence against fungal infections. Curr. Opin. Microbiol. 2011, 14:392-399.
46. Dupuy A.G., Caron E. Integrin-dependent phagocytosis: spreading from microadhesion to new concepts. J. Cell Sci. 2008, 121:1773-1783.
47. Ebanks J.P., Koshoffer A., Wickett R.R., Schwemberger S., Babcock G., Hakozaki T., Boissy R.E. Epidermal keratinocytes from light vs. dark skin exhibit differential degradation of melanosomes. J. Invest. Dermatol. 2011, 131:1226-1233.
48. Elliott M.R., Zheng S., Park D., Woodson R.I., Reardon M.A., Juncadella I.J., Kinchen J.M., Zhang J., Lysiak J.J., Ravichandran K.S. Unexpected requirement for ELMO1 in clearance of apoptotic germ cells in vivo. Nature 2010, 467:333-337.
49. Ensslin M.A., Shur B.D. The EGF repeat and discoidin domain protein, SED1/MFG-E8, is required for mammary gland branching morphogenesis. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:2715-2720.
50. Everts V., van der Zee E., Creemers L., Beertsen W. Phagocytosis and intracellular digestion of collagen, its role in turnover and remodelling. Histochem. J. 1996, 28:229-245.
51. Feire A.L., Koss H., Compton T. Cellular integrins function as entry receptors for human cytomegalovirus via a highly conserved disintegrin-like domain. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:15470-15475.
52. Finnemann S.C. Focal adhesion kinase promotes phagocytosis of integrin-bound photoreceptors. EMBO J. 2003, 22:4143-4154.
53. Flannagan R.S., Jaumouille V., Grinstein S. The cell biology of phagocytosis. Annu. Rev. Pathol. 2012, 7:61-98.
54. Fleming F.E., Graham K.L., Takada Y., Coulson B.S. Determinants of the specificity of rotavirus interactions with the alpha2beta1 integrin. J. Biol. Chem. 2011, 286:6165-6174.
55. Fricker M., Neher J.J., Zhao J.W., Thery C., Tolkovsky A.M., Brown G.C. MFG-E8 mediates primary phagocytosis of viable neurons during neuroinflammation. J. Neurosci. 2012, 32:2657-2666.
56. Fukuda K., Gupta S., Chen K., Wu C., Qin J. The pseudoactive site of ILK is essential for its binding to alpha-Parvin and localization to focal adhesions. Mol. Cell 2009, 36:819-830.
57. Fukuda K., Knight J.D., Piszczek G., Kothary R., Qin J. Biochemical, proteomic, structural, and thermodynamic characterizations of integrin-linked kinase (ILK): cross-validation of the pseudokinase. J. Biol. Chem. 2011, 286:21886-21895.
58. Fuller A.D., Van Eldik L.J. MFG-E8 regulates microglial phagocytosis of apoptotic neurons. J. Neuroimmune Pharmacol. 2008, 3:246-256.
59. Gaipl U.S., Franz S., Voll R.E., Sheriff A., Kalden J.R., Herrmann M. Defects in the disposal of dying cells lead to autoimmunity. Curr. Rheumatol. Rep. 2004, 6:401-407.
60. Gaipl U.S., Voll R.E., Sheriff A., Franz S., Kalden J.R., Herrmann M. Impaired clearance of dying cells in systemic lupus erythematosus. Autoimmun. Rev. 2005, 4:189-194.
61. Gibbs D., Kitamoto J., williams D.S. Abnormal phagocytosis by retinal pigmented epithelium that lacks myosin VIIa, the Usher syndrom 1B protein. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:6481-6486.
62. Grashoff C., Aszodi A., Sakai T., Hunziker E.B., Fassler R. Integrin-linked kinase regulates chondrocyte shape and proliferation. EMBO Rep. 2003, 4:432-438.
63. Griffin F.M., Griffin J.A., Leider J.E., Silverstein S.C. Studies on the mechanism of phagocytosis. I. Requirements for circumferential attachment of particle-bound ligands to specific receptors on the macrophage plasma membrane. J. Exp. Med. 1975, 142:1263-1282.
64. Groves E., Dart A.E., Covarelli V., Caron E. Molecular mechanisms of phagocytic uptake in mammalian cells. Cell. Mol. Life Sci. 2008, 65:1957-1976.
65. Hanayama R., Nagata S. Impaired involution of mammary glands in the absence of milk fat globule EGF factor 8. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:16886-16891.
66. Hanayama R., Tanaka M., Miwa K., Shinohara A., Iwamatsu A., Nagata S. Identification of a factor that links apoptotic cells to phagocytes. Nature 2002, 417:182-187.
67. Hanayama R., Tanaka M., Miyasaka K., Aozasa K., Koike M., Uchiyama W., Nagata S. Autoimmune disease and impaired uptake of apoptotic cells in MFG-E8-deficient mice. Science 2004, 304:1147-1150.
68. Hannigan G.E., Leung-Hagesteijn C., Fitz-Gibbon L., Coppolino M.G., Radeva G., Filmus J., Bell J.C., Dedhar S. Regulation of cell adhesion and anchorage-dependent cell growth by a new beta 1-integrin-linked protein kinase. Nature 1996, 379:91-96.
69. Harburger D.S., Calderwood D.A. Integrin signalling at a glance. J. Cell Sci. 2009, 122:159-163.
70. Hauck C.R., Ohlsen K. Sticky connections: extracellular matrix protein recognition and integrin-mediated cellular invasion by Staphylococcus aureus. Curr. Opin. Microbiol. 2006, 9:5-11.
71. Ho E., Dagnino L. Epidermal growth factor induction of front-rear polarity and migration in keratinocytes is mediated by integrin-linked kinase and ELMO2. Mol. Biol. Cell 2012, 23:492-502.
72. Ho E., Irvine T., Vilk G.J., Lajoie G., Ravichandran K.S., D'Souza S.J., Dagnino L. Integrin-linked kinase interactions with ELMO2 modulate cell polarity. Mol. Biol. Cell 2009, 20:3033-3043.
73. Hodge S., Hodge G., Scicchitano R., Reynolds P.N., Holmes M. Alveolar macrophages from subjects with chronic obstructive pulmonary disease are deficient in their ability to phagocytose apoptotic airway epithelial cells. Immunol. Cell Biol. 2003, 81:289-296.
74. Hoffmann C., Ohlsen K., Hauck C.R. Integrin-mediated uptake of fibronectin-binding bacteria. Eur. J. Cell Biol. 2011, 90:891-896.
75. Hudson K.J., Bliska J.B., Bouton A.H. Distinct mechanisms of integrin binding by Yersinia pseudotuberculosis adhesins determine the phagocytic response of host macrophages. Cell. Microbiol. 2005, 7:1474-1489.
76. Hughes R.C. Galectins as modulators of cell adhesion. Biochimie 2001, 83:667-676.
77. Humphries M.J. Insights into integrin-ligand binding and activation from the first crystal structure. Arthritis Res. 2002, 4(Suppl. 3):S69-S78.
78. Hynes R.O. Integrins: bidirectional, allosteric signaling machines. Cell 2002, 110:673-687.
79. Isberg R.R., Leong J.M. Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell 1990, 60:861-871.
80. Janssen W.J., McPhillips K.A., Dickinson M.G., Linderman D.J., Morimoto K., Xiao Y.Q., Oldham K.M., Vandivier R.W., Henson P.M., Gardai S.J. Surfactant proteins A and D suppress alveolar macrophage phagocytosis via interaction with SIRP alpha. Am. J. Respir. Crit. Care Med. 2008, 178:158-167.
81. Jiang J.X., Chen X., Hsu D.K., Baghy K., Serizawa N., Scott F., Takada Y., Takada Y., Fukada H., Chen J., Devaraj S., Adamson R., Liu F.T., Torok N.J. Galectin-3 modulates phagocytosis-induced stellate cell activation and liver fibrosis in vivo. Am. J. Physiol. Gastrointest. Liver Physiol. 2012, 302:G439-G446.
82. Kaplan G. Differences in the mode of phagocytosis with Fc and C3 receptors in macrophages. Scand. J. Immunol. 1977, 6:797-807.
83. Kaufmann S.H., Walker B.D. Host-pathogen interactions. Curr. Opin. Immunol. 2006, 18:371-373.
84. Kim M., Ogawa M., Fujita Y., Yoshikawa Y., Nagai T., Koyama T., Nagai S., Lange A., Fassler R., Sasakawa C. Bacteria hijack integrin-linked kinase to stabilize focal adhesions and block cell detachment. Nature 2009, 459:578-582..
85. Kim S., Park S.-Y., Kim S.-Y., Bae D.-J., Pyo J.-H., Hong M., Kim I.-S. Cross talk between engulfment receptors Stabilin-2 and integrin αVβ5 orchestrates engulfment of phosphatidylserine-exposed erythrocytes. Mol. Biol. Cell 2012, 32:2698-2708.
86. Kinchen J.M., Doukoumetzidis K., Almendinger J., Stergiou L., Tosello-Trampont A., Sifri C.D., Hengartner M.O., Ravichandran K.S. A pathway for phagosome maturation during engulfment of apoptotic cells. Nat. Cell Biol. 2008, 10:556-566.
87. Kinchen J.M., Ravichandran K.S. Phagosome maturation: going through the acid test. Nat. Rev. Mol. Cell Biol. 2008, 9:781-795.
88. Knowles G.C., McKeown M., Sodek J., McCulloch C.A. Mechanism of collagen phagocytosis by human gingival fibroblasts: Importance of collagen structure in cell recognition and internalization. J. Cell Sci. 1991, 98:551-558.
89. Kobayashi N., Karisola P., Pena-Cruz V., Dorfman D.M., Jinushi M., Umetsu S.E., Butte M.J., Nagumo H., Chernova I., Zhu B., Sharpe A.H., Ito S., Dranoff G., Kaplan G.G., Casasnovas J.M., Umetsu D.T., Dekruyff R.H., Freeman G.J. TIM-1 and TIM-4 glycoproteins bind phosphatidylserine and mediate uptake of apoptotic cells. Immunity 2007, 27:927-940.
90. Kreiselmeier N.E., Kraynack N.C., Corey D.A., Kelley T.J. Statin-mediated correction of STAT1 signaling and inducible nitric oxide synthase expression in cystic fibrosis epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 2003, 285:L1286-L1295.
91. Kwok T., Zabler D., Urman S., Rohde M., Hartig R., Wessler S., Misselwitz R., Berger J., Sewald N., Konig W., Backert S. Helicobacter exploits integrin for type IV secretion and kinase activation. Nature 2007, 449:862-866.
92. Lacy-Hulbert A., Smith A.M., Tissire H., Barry M., Crowley D., Bronson R.T., Roes J.T., Savill J.S., Hynes R.O. Ulcerative colitis and autoimmunity induced by loss of myeloid alphav integrins. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:15823-15828.
93. Lange A., Wickstrom S.A., Jakobson M., Zent R., Sainio K., Fassler R. Integrin-linked kinase is an adaptor with essential functions during mouse development. Nature 2009, 461:1002-1006.
94. LaVail M. Rod outer segment disc shedding in rat retina: relationship to cyclic lighting. Science 1976, 194:1071-1074.
95. Law A.L. Annexin A2 regulates phagocytosis of photoreceptors outer segments in the mouse retina. Mol. Biol. Cell 2009, 20:3896-3904.
96. Law A.L., Nandrot E.F. On your marks.get bound.internalize!. Adv. Exp. Med. Biol. 2012, 723:717-722.
97. Lee H., Overall C.M., McCulloch C.A., Sodek J. A critical role for the membrane-type 1 matrix metalloproteinase in collagen phagocytosis. Mol. Biol. Cell 2006, 17:4812-4826.
98. Li E., Stupack D., Bokoch G.M., Nemerow G.R. Adenovirus endocytosis requires actin cytoskeleton reorganization mediated by Rho family GTPases. J. Virol. 1998, 72:8806-8812.
99. Li E., Stupack D., Klemke R., Cheresh D.A., Nemerow G.R. Adenovirus endocytosis via alpha(v) integrins requires phosphoinositide-3-OH kinase. J. Virol. 1998, 72:2055-2061.
100. Lorand L., Graham R.M. Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat. Rev. Mol. Cell Biol. 2003, 4:140-156.
101. Mao Y., Finnemann S.C. Essential diurnal Rac1 activation during retinal phagocytosis requires alphavbeta5 integrin but not tyrosine kinases focal adhesion kinase or Mer tyrosine kinase. Mol. Biol. Cell 2012, 23:1104-1114.
102. Margadant C., Monsuur H.N., Norman J.C., Sonnenberg A. Mechanisms of integrin activation and trafficking. Curr. Opin. Cell Biol. 2011, 23:607-614.
103. Maydan M., McDonald P.C., Sanghera J., Yan J., Rallis C., Pinchin S., Hannigan G.E., Foster L.J., Ish-Horowicz D., Walsh M.P., Dedhar S. Integrin-linked kinase is a functional Mn2+-dependent protein kinase that regulates glycogen synthase kinase-3beta (GSK-3beta) phosphorylation. PLoS One 2010, 5:e12356.
104. McGaw W.T., Ten Cate A.R. A role for collagen phagocytosis by fibroblasts in scar remodeling: an ultrastructural stereologic study. J. Invest. Dermatol. 1983, 81:375-378.
105. Menzies B.E., Kourteva Y., Kaiser A.B., Kernodle D.S. Inhibition of staphylococcal wound infection and potentiation of antibiotic prophylaxis by a recombinant fragment of the fibronectin-binding protein of Staphylococcus aureus. J. Infect. Dis. 2002, 185:937-943.
106. Nakrieko K.A., Rudkouskaya A., Irvine T.S., D'Souza S.J., Dagnino L. Targeted inactivation of integrin-linked kinase in hair follicle stem cells reveals an important modulatory role in skin repair after injury. Mol. Biol. Cell 2011, 22:2532-2540.
107. Nakrieko K.A., Vespa A., Mason D., Irvine T., D'Souza S.J.A., Dagnino L. Modulation of integrin-linked kinase cytoplasmic shuttling by ILKAP and CRM1. Cell Cycle 2008, 7:2157-2166.
108. Nandrot E.F., Anand M., Almeida D., Atabai K., Sheppard D., Finnemann S.C. Essential role for MFG-E8 as ligand for alphavbeta5 integrin in diurnal retinal phagocytosis. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:12005-12010.
109. Nandrot E.F., Kim Y., Brodie S.E., Huang X., Sheppard D., Finnemann S.C. Loss of synchronized retinal phagocytosis and age-related blindness in mice lacking alphavbeta5 integrin. J. Exp. Med. 2004, 200:1539-1545.
110. Neher J.J., Neniskyte U., Zhao J.W., Bal-Price A., Tolkovsky A.M., Brown G.C. Inhibition of microglial phagocytosis is sufficient to prevent inflammatory neuronal death. J. Immunol. 2011, 186:4973-4983.
111. Neniskyte U., Neher J.J., Brown G.C. Neuronal death induced by nanomolar amyloid beta is mediated by primary phagocytosis of neurons by microglia. J. Biol. Chem. 2011, 286:39904-39913.
112. Newlaczyl A.U., Yu L.G. Galectin-3-a jack-of-all-trades in cancer. Cancer Lett. 2011, 313:123-128.
113. Niedergang F., Chavrier P. Regulation of phagocytosis by Rho GTPases. Curr. Top. Microbiol. Immunol. 2005, 291:43-60.
114. Nikolopoulos S.N., Turner C.E. Integrin-linked kinase (ILK) binding to paxillin LD1 motif regulates ILK localization to focal adhesions. J. Biol. Chem. 2001, 276:23499-23505.
115. Nikolopoulos S.N., Turner C.E. Molecular dissection of actopaxin-integrin-linked kinase-paxillin interactions and their role in subcellular localization. J. Biol. Chem. 2002, 277:1568-1575.
116. Nobbs A.H., Lamont R.J., Jenkinson H.F. Streptococcus adherence and colonization. Microbiol. Mol. Biol. Rev. 2009, 73:407-450. (Table of Contents).
117. Olazabal I.M., Caron E., May R.C., Schilling K., Knecht D.A., Machesky L.M. Rho-kinase and myosin-II control phagocytic cup formation during CR, but not FcgammaR, phagocytosis. Curr. Biol. 2002, 12:1413-1418.
118. Olski T.M., Noegel A.A., Korembaum E. Parvin, a 42 kDa focal adhesion protein, related to the α-actinin superfamily. J. Cell Sci. 2001, 114:525-538.
119. Park D., Ravichandran K.S. Emerging roles of brain-specific angiogenesis inhibitor 1. Adv. Exp. Med. Biol. 2010, 706:167-178.
120. Parry C., Bell S., Minson T., Browne H. Herpes simplex virus type 1 glycoprotein H binds to alphavbeta3 integrins. J. Gen. Virol. 2005, 86:7-10.
121. Patel P.C., Harrison R.E. Membrane ruffles capture C3bi-opsonized particles in activated macrophages. Mol. Biol. Cell 2008, 19:4628-4639.
122. Peiser L., Gough P.J., Kodama T., Gordon S. Macrophage class A scavenger receptor-mediated phagocytosis of Escherichia coli: role of cell heterogeneity, microbial strain, and culture conditions in vitro. Infect. Immun. 2000, 68:1953-1963.
123. Prashar A., Bhatia S., Tabatabaeiyazdi Z., Duncan C., Garduno R.A., Tang P., Low D.E., Guyard C., Terebiznik M.R. Mechanism of invasion of lung epithelial cells by Filamentous Legionella pneumophila. Cell. Microbiol 2012, 14:1632-1655.
124. Qin S., Rodrigues G.A. Roles of alphavbeta5, FAK and MerTK in oxidative stress inhibition of RPE cell phagocytosis. Exp. Eye Res. 2012, 94:63-70.
125. Que Y.A., Haefliger J.A., Piroth L., Francois P., Widmer E., Entenza J.M., Sinha B., Herrmann M., Francioli P., Vaudaux P., Moreillon P. Fibrinogen and fibronectin binding cooperate for valve infection and invasion in Staphylococcus aureus experimental endocarditis. J. Exp. Med. 2005, 201:1627-1635.
126. Ravichandran K.S. Find-me and eat-me signals in apoptotic cell clearance: progress and conundrums. J. Exp. Med. 2010, 207:1807-1817.
127. Ravichandran K.S. Beginnings of a good apoptotic meal: the find-me and eat-me signaling pathways. Immunity 2011, 35:445-455.
128. Raymond A., Ensslin M.A., Shur B.D. SED1/MFG-E8: a bi-motif protein that orchestrates diverse cellular interactions. J. Cell Biochem. 2009, 106:957-966.
129. Richens T.R., Linderman D.J., Horstmann S.A., Lambert C., Xiao Y.Q., Keith R.L., Boe D.M., Morimoto K., Bowler R.P., Day B.J., Janssen W.J., Henson P.M., Vandivier R.W. Cigarette smoke impairs clearance of apoptotic cells through oxidant-dependent activation of RhoA. Am. J. Respir. Crit. Care Med. 2009, 179:1011-1021.
130. Rodriguez-Manzanet R., Sanjuan M.A., Wu H.Y., Quintana F.J., Xiao S., Anderson A.C., Weiner H.L., Green D.R., Kuchroo V.K. T and B cell hyperactivity and autoimmunity associated with niche-specific defects in apoptotic body clearance in TIM-4-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:8706-8711.
131. Ross G.D., Reed W., Dalzell J.G., Becker S.E., Hogg N. Macrophage cytoskeleton association with CR3 and CR4 regulates receptor mobility and phagocytosis of iC3b-opsonized erythrocytes. J. Leukoc. Biol. 1992, 51:109-117.
132. Sakai T., Li S., Dicheva D., Grashoff C., Sakai K., Kostka G., Braun A., Pfeifer A., Yurchenco P.D., Fassler R. Integrin-linked kinase (ILK) is required for polarizing the epiblast, cell adhesion and controlling actin accumulation. Genes Dev. 2003, 17:926-940.
133. Savill J., Dransfield I., Hogg N., Haslett C. Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis. Nature 1990, 343:170-173.
134. Savill J., Fadok V.A. Corpse clearance defines the meaning of cell death. Nature 2000, 407:784-788.
135. Sayedyahossein S., Nini L., Irvine T., Dagnino L. FASEB J 2012, 26:4218-4229.
136. Scott G., Leopardi S., Parker L., Babiarz L., Seiberg M., Han R. The proteinase-activated receptor-2 mediates phagocytosis in a Rho-dependent manner in human keratinocytes. J. Invest. Dermatol. 2003, 121:529-541.
137. Sharlow E.R., Paine C.S., Babiarz L., Eisinger M., Shapiro S., Seiberg M. The protease-activated receptor-2 upregulates keratinocyte phagocytosis. J. Cell Sci. 2000, 113(Pt 17):3093-3101.
138. Shattil S.J., Kim C., Ginsberg M.H. The final steps of integrin activation: the end game. Nat. Rev. Mol. Cell Biol. 2010, 11:288-300.
139. Siemens N., Patenge N., Otto J., Fiedler T., Kreikemeyer B. Streptococcus pyogenes M49 plasminogen/plasmin binding facilitates keratinocyte invasion via integrin-integrin-linked kinase (ILK) pathways and protects from macrophage killing. J. Biol. Chem. 2011, 286:21612-21622.
140. Sindrilaru A., Peters T., Schymeinsky J., Oreshkova T., Wang H., Gompf A., Mannella F., Wlaschek M., Sunderkotter C., Rudolph K.L., Walzog B., Bustelo X.R., Fischer K.D., Scharffetter-Kochanek K. Wound healing defect ofVav3-/- mice due to impaired {beta}2-integrin-dependent macrophage phagocytosis of apoptotic neutrophils. Blood 2009, 113:5266-5276.
141. Sinha B., Fraunholz M. Staphylococcus aureus host cell invasion and post-invasion events. Int. J. Med. Microbiol. 2010, 300:170-175.
142. Stewart P.L., Nemerow G.R. Cell integrins: commonly used receptors for diverse viral pathogens. Trends Microbiol. 2007, 15:500-507.
143. Strick D.J., Feng W., Vollrath D. Mertk drives myosin II redistribution during retinal pigment epithelial phagocytosis. Invest. Ophthalmol. Vis. Sci. 2009, 50:2427-2435.
144. Swanson J.A. Shaping cups into phagosomes and macropinosomes. Nat. Rev. Mol. Cell Biol. 2008, 9:639-649.
145. Terpstra L., Prud'homme J., Arabian A., Takeda S., Karsenty G., Dedhar S., St-Arnaud R. Reduced chondrocyte proliferation and chondrodysplasia in mice lacking the integrin-linked kinase in chondrocytes. J. Cell Biol. 2003, 162:139-148.
146. Tiwari V., Shukla D. Nonprofessional phagocytosis can facilitate herpesvirus entry into ocular cells. Clin. Dev. Immunol. 2012, 2012:651691.
147. Tu Y., Huang Y., Zhang Y., Hua Y., Wu C. A new focal adhesion protein that interacts with integrin-linked kinase and regulates cell adhesion and spreading. J. Cell Biol. 2001, 153:585-598.
148. Tu Y., Li F., Goicoechea S., Wu C. The LIM-only protein PINCH directly interacts with integrin-linked-kinase and is recruited to integrin-rich sites in spreading cells. Mol. Cell. Biol. 1999, 19:2425-2434.
149. Tzircotis G., Braga V.M., Caron E. RhoG is required for both FcgammaR- and CR3-mediated phagocytosis. J. Cell Sci. 2011, 124:2897-2902.
150. Van Den Bossche K., Naeyaert J.-M., Lambert J. The quest for the mechanism of melanin transfer. Traffic 2006, 7:769-778.
151. Vandivier R.W., Richens T.R., Horstmann S.A., deCathelineau A.M., Ghosh M., Reynolds S.D., Xiao Y.Q., Riches D.W., Plumb J., Vachon E., Downey G.P., Henson P.M. Dysfunctional cystic fibrosis transmembrane conductance regulator inhibits phagocytosis of apoptotic cells with proinflammatory consequences. Am. J. Physiol. Lung Cell. Mol. Physiol. 2009, 297:L677-L686.
152. Vicente-Manzanares M., Ma X., Adelstein R.S., Horwitz A.R. Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat. Rev. Mol. Cell Biol. 2009, 10:778-790.
153. Virador V.M., Muller J., Wu X., Abdel-Malek Z.A., Yu Z.X., Ferrans V.J., Kobayashi N., Wakamatsu K., Ito S., Hammer J.A., Hearing V.J. Influence of alpha-melanocyte-stimulating hormone and ultraviolet radiation on the transfer of melanosomes to keratinocytes. FASEB J. 2002, 16:105-107.
154. Wang B., Yurecko R.S., Dedhar S., Cleary P.P. Integrin-linked kinase is an essential link between integrins and uptake of bacterial pathogens by epithelial cells. Cell. Microbiol. 2006, 8:257-266.
155. Wang T., Ming Z., Xiaochun W., Hong W. Rab7: role of its protein interaction cascades in endo-lysosomal traffic. Cell Signal. 2011, 23:516-521.
156. Wang X., Huang D.Y., Huong S.M., Huang E.S. Integrin alphavbeta3 is a coreceptor for human cytomegalovirus. Nat. Med. 2005, 11:515-521.
157. Watarai M., Funato S., Sasakawa C. Interaction of Ipa proteins of Shigella flexneri with alpha5beta1 integrin promotes entry of the bacteria into mammalian cells. J. Exp. Med. 1996, 183:991-999.
158. Wickham T.J., Mathias P., Cheresh D.A., Nemerow G.R. Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment. Cell 1993, 73:309-319.
159. Wu Y., Singh S., Georgescu M., Birge R.B. A role for Mer tyrosine kinase in alpjavbeta5 integrin-mediated phagocytosis of apoptotic cells. J. Cell Sci. 2005, 118:539-553.
160. Yamaji S., Suzuki A., Sugiyama Y., Koide Y.-I., Yoshida M., Kanamori H., Mohri H., Ohno S., Ishigatsubo Y. A novel integrin-linked kinase-binding protein, affixin, is involved in the early stage of cell-substrate interaction. J. Cell Biol. 2001, 153:1251-1264.
161. Young R.W., Bok D. Participation of the retinal pigment epithelium in the rod outer segment renewal process. J. Cell Biol. 1969, 42:392-403.
162. Zaidel-Bar R., Itzkovitz S., Ma'ayan A., Iyengar R., Geiger B. Functional atlas of the integrin adhesome. Nat. Cell Biol. 2007, 9:858-867.
163. Zanoni I., Ostuni R., Marek L.R., Barresi S., Barbalat R., Barton G.M., Granucci F., Kagan J.C. CD14 controls the LPS-induced endocytosis of Toll-like receptor 4. Cell 2011, 147:868-880.
164. Zhang Y., Guo L., Chen K., Wu C. A critical role of the PINCH-integrin-linked kinase interaction in the regulation of cell shape change and migration. J. Biol. Chem. 2002, 277:318-326.
165. Zhao J., Guan J.L. Signal transduction by focal adhesion kinase in cancer. Cancer Metastasis Rev. 2009, 28:35-49.