Mechanisms of apical-basal axis orientation and epithelial lumen positioning

Trends in Cell Biology

Volumn 25, Issue 8, 2015, Pages 476-485

  Overeem, Arend W ^a   Bryant, David M ^b   van IJzendoorn, Sven C D ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Apical lumen; Cell polarity; Extracellular matrix; Rab11; Recycling endosome

Indexed keywords

APICAL BASAL POLARITY AXIS; APICAL MEMBRANE; CELL DIVISION; CELL MEMBRANE; CELL MIGRATION; CELLULAR DISTRIBUTION; CYTOKINESIS; ENDOSOME; EPITHELIUM BASAL CELL; EXTRACELLULAR MATRIX; HUMAN; INTRACELLULAR SIGNALING; MICROVILLUS; NONHUMAN; ORIENTATION; PRIORITY JOURNAL; REVIEW; ANIMAL; CELL POLARITY; EPITHELIUM CELL; PHYSIOLOGY; SIGNAL TRANSDUCTION; SPINDLE APPARATUS;

ANIMALIA;

ANIMALS; CELL MEMBRANE; CELL POLARITY; CYTOKINESIS; EPITHELIAL CELLS; HUMANS; SIGNAL TRANSDUCTION; SPINDLE APPARATUS;

EID: 84937734647     PISSN: 09628924     EISSN: 18793088     Source Type: Journal    
DOI: 10.1016/j.tcb.2015.04.002     Document Type: Review

References (102)

1. Bryant D.M., et al. A molecular network for de novo generation of the apical surface and lumen. Nat. Cell Biol. 2010, 12:1035-1045.
2. Bryant D.M., et al. A molecular switch for the orientation of epithelial cell polarization. Dev. Cell 2014, 31:171-187.
3. Datta A., et al. Molecular regulation of lumen morphogenesis. Curr. Biol. 2011, 21:R126-R136.
4. Ferrari A., et al. ROCK-mediated contractility, tight junctions and channels contribute to the conversion of a preapical patch into apical surface during isochoric lumen initiation. J. Cell Sci. 2008, 121:3649-3663.
5. Jaffe A.B., et al. Cdc42 controls spindle orientation to position the apical surface during epithelial morphogenesis. J. Cell Biol. 2008, 183:625-633.
6. Martin-Belmonte F., Mostov K. Phosphoinositides control epithelial development. Cell Cycle 2007, 6:1957-1961.
7. Schlüter M.A., et al. Trafficking of Crumbs3 during cytokinesis is crucial for lumen formation. Mol. Biol. Cell 2009, 20:4652-4663.
8. Fu D., et al. Bile acid stimulates hepatocyte polarization through a cAMP-Epac-MEK-LKB1-AMPK pathway. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:1403-1408.
9. Herrema H., et al. Rho kinase, myosin-II, and p42/44 MAPK control extracellular matrix-mediated apical bile canalicular lumen morphogenesis in HepG2 cells. Mol. Biol. Cell 2006, 17:3291-3303.
10. Slim C.L., et al. Par1b induces asymmetric inheritance of plasma membrane domains via LGN-dependent mitotic spindle orientation in proliferating hepatocytes. PLoS Biol. 2013, 11:e1001739.
11. Lázaro-Diéguez F., et al. Par1b links lumen polarity with LGN-NuMA positioning for distinct epithelial cell division phenotypes. J. Cell Biol. 2013, 203:251-264.
12. Wang T., et al. Cytokinesis defines a spatial landmark for hepatocyte polarization and apical lumen formation. J. Cell Sci. 2014, 127:2483-2492.
13. Fu D., et al. Regulation of bile canalicular network formation and maintenance by AMP-activated protein kinase and LKB1. J. Cell Sci. 2010, 123:3294-3302.
14. Akhtar N., Streuli C.H. An integrin-ILK-microtubule network orients cell polarity and lumen formation in glandular epithelium. Nat. Cell Biol. 2013, 15:17-27.
15. Wodarz A., et al. Expression of crumbs confers apical character on plasma membrane domains of ectodermal epithelia of Drosophila. Cell 1995, 82:67-76.
16. Nielsen J.S., et al. The CD34-related molecule podocalyxin is a potent inducer of microvillus formation. PLoS ONE 2007, 2:e237.
17. Hobdy-Henderson K.C., et al. Dynamics of the apical plasma membrane recycling system during cell division. Traffic 2003, 4:681-693.
18. Yu W., et al. Involvement of RhoA, ROCK I and myosin II in inverted orientation of epithelial polarity. EMBO Rep. 2008, 9:923-929.
19. Myllymäki S.M., et al. Two distinct integrin-mediated mechanisms contribute to apical lumen formation in epithelial cells. PLoS ONE 2011, 6:e19453.
20. Yu W., et al. Beta1-integrin orients epithelial polarity via Rac1 and laminin. Mol. Biol. Cell 2005, 16:433-445.
21. O'Brien L.E., et al. Rac1 orientates epithelial apical polarity through effects on basolateral laminin assembly. Nat. Cell Biol. 2001, 3:831-838.
22. Liu K.D., et al. Rac1 is required for reorientation of polarity and lumen formation through a PI 3-kinase-dependent pathway. Am. J. Physiol. Renal Physiol. 2007, 293:F1633-F1640.
23. Peng J., et al. Phosphoinositide 3-kinase p110δ promotes lumen formation through the enhancement of apico-basal polarity and basal membrane organization. Nat. Commun. 2015, 6:5937.
24. Xu R., et al. Laminin regulates PI3K basal localization and activation to sustain STAT5 activation. Cell Cycle 2010, 9:4315-4322.
25. Monteleon C.L., et al. Establishing epithelial glandular polarity: interlinked roles for ARF6, Rac1, and the matrix microenvironment. Mol. Biol. Cell 2012, 23:4495-4505.
26. Manninen A. Epithelial polarity - generating and integrating signals from the ECM with integrins. Exp. Cell Res. 2015, Published January 15, 2015. 10.1016/j.yexcr.2015.01.003.
27. Masuda-Hirata M., et al. Intracellular polarity protein PAR-1 regulates extracellular laminin assembly by regulating the dystroglycan complex. Genes Cells 2009, 14:835-850.
28. Lewandowski K.T., Piwnica-Worms H. Phosphorylation of the E3 ubiquitin ligase RNF41 by the kinase Par-1b is required for epithelial cell polarity. J. Cell Sci. 2014, 127:315-327.
29. Cohen D., et al. The serine/threonine kinase Par1b regulates epithelial lumen polarity via IRSp53-mediated cell-ECM signaling. J. Cell Biol. 2011, 192:525-540.
30. Cohen D., et al. Mammalian PAR-1 determines epithelial lumen polarity by organizing the microtubule cytoskeleton. J. Cell Biol. 2004, 164:717-727.
31. Daley W.P., et al. ROCK1-directed basement membrane positioning coordinates epithelial tissue polarity. Development 2012, 139:411-422.
32. Madrid R., et al. The formin INF2 regulates basolateral-to-apical transcytosis and lumen formation in association with Cdc42 and MAL2. Dev. Cell 2010, 18:814-827.
33. Zeigerer A., et al. Rab5 is necessary for the biogenesis of the endolysosomal system in vivo. Nature 2012, 485:465-470.
34. Bigorgne A.E., et al. TTC7A mutations disrupt intestinal epithelial apicobasal polarity. J. Clin. Invest. 2014, 124:328-337.
35. Desclozeaux M., et al. Active Rab11 and functional recycling endosome are required for E-cadherin trafficking and lumen formation during epithelial morphogenesis. Am. J. Physiol. Cell Physiol. 2008, 295:C545-C556.
36. Casanova J.E., et al. Association of Rab25 and Rab11a with the apical recycling system of polarized Madin-Darby canine kidney cells. Mol. Biol. Cell 1999, 10:47-61.
37. Rodríguez-Fraticelli A.E., et al. Cell confinement controls centrosome positioning and lumen initiation during epithelial morphogenesis. J. Cell Biol. 2012, 198:1011-1023.
38. Rodríguez-Fraticelli A.E., Martín-Belmonte F. Mechanical control of epithelial lumen formation. Small GTPases 2013, 4:136-140.
39. Roland J.T., et al. Rab GTPase-Myo5B complexes control membrane recycling and epithelial polarization. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:2789-2794.
40. Li D., et al. FIP5 phosphorylation during mitosis regulates apical trafficking and lumenogenesis. EMBO Rep. 2014, 15:428-437.
41. Wakabayashi Y., et al. Rab11a and myosin Vb are required for bile canalicular formation in WIF-B9 cells. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:15087-15092.
42. Sobajima T., et al. Rab11a is required for apical protein localisation in the intestine. Biol. Open 2014, 4:86-94.
43. Sato T., et al. The Rab8 GTPase regulates apical protein localization in intestinal cells. Nature 2007, 448:366-369.
44. Martin-Belmonte F., Mostov K. Regulation of cell polarity during epithelial morphogenesis. Curr. Opin. Cell Biol. 2008, 20:227-234.
45. Dhekne H.S., et al. Myosin Vb and Rab11a regulate phosphorylation of ezrin in enterocytes. J. Cell Sci. 2014, 127:1007-1017.
46. Kravtsov D., et al. Myosin 5b loss of function leads to defects in polarized signaling: implication for microvillus inclusion disease pathogenesis and treatment. Am. J. Physiol. Gastrointest. Liver Physiol. 2014, 307:G992-G1001.
47. Gálvez-Santisteban M., et al. Synaptotagmin-like proteins control the formation of a single apical membrane domain in epithelial cells. Nat. Cell Biol. 2012, 14:838-849.
48. Treyer A., Müsch A. Hepatocyte polarity. Compr. Physiol. 2013, 3:243-287.
49. Fukuda M., et al. Novel splicing isoforms of synaptotagmin-like proteins 2 and 3: identification of the Slp homology domain. Biochem. Biophys. Res. Commun. 2001, 283:513-519.
50. Homolya L., et al. LKB1/AMPK and PKA control ABCB11 trafficking and polarization in hepatocytes. PLoS ONE 2014, 9:e91921.
51. Woods A., et al. LKB1 is required for hepatic bile acid transport and canalicular membrane integrity in mice. Biochem. J. 2011, 434:49-60.
52. Winter J.F., et al. Caenorhabditis elegans screen reveals role of PAR-5 in RAB-11-recycling endosome positioning and apicobasal cell polarity. Nat. Cell Biol. 2012, 14:666-676.
53. Zhang H., et al. Clathrin and AP-1 regulate apical polarity and lumen formation during C. elegans tubulogenesis. Development 2012, 139:2071-2083.
54. Zhang H., et al. Vesicular sorting controls the polarity of expanding membranes in the C. elegans intestine. Worm 2013, 2:e23702.
55. Shafaq-Zadah M., et al. AP-1 is required for the maintenance of apico-basal polarity in the C. elegans intestine. Development 2012, 139:2061-2070.
56. Khan L.A., et al. Intracellular lumen extension requires ERM-1-dependent apical membrane expansion and AQP-8-mediated flux. Nat. Cell Biol. 2013, 15:143-156.
57. Müller T., et al. MYO5B mutations cause microvillus inclusion disease and disrupt epithelial cell polarity. Nat. Genet. 2008, 40:1163-1165.
58. Szperl A.M., et al. Functional characterization of mutations in the myosin Vb gene associated with microvillus inclusion disease. J. Pediatr. Gastroenterol. Nutr. 2011, 52:307-313.
59. Wiegerinck C.L., et al. Loss of syntaxin 3 causes variant microvillus inclusion disease. Gastroenterology 2014, 147:65-68.
60. Cutz E., et al. Microvillus inclusion disease: an inherited defect of brush-border assembly and differentiation. N. Engl. J. Med. 1989, 320:646-651.
61. Gilbert T., Rodriguez-Boulan E. Induction of vacuolar apical compartments in the Caco-2 intestinal epithelial cell line. J. Cell Sci. 1991, 100:451-458.
62. Vega-Salas D.E., et al. Vacuolar apical compartment (VAC) in breast carcinoma cell lines (MCF-7 and T47D): failure of the cell-cell regulated exocytosis mechanism of apical membrane. Differ. Res. Biol. Divers. 1993, 54:131-141.
63. Low S.H., et al. Intracellular redirection of plasma membrane trafficking after loss of epithelial cell polarity. Mol. Biol. Cell 2000, 11:3045-3060.
64. Knowles B.C., et al. Myosin Vb uncoupling from RAB8A and RAB11A elicits microvillus inclusion disease. J. Clin. Invest. 2014, 124:2947-2962.
65. Ameen N.A., Salas P.J. Microvillus inclusion disease: a genetic defect affecting apical membrane protein traffic in intestinal epithelium. Traffic 2000, 1:76-83.
66. Barker N., et al. Tissue-resident adult stem cell populations of rapidly self-renewing organs. Cell Stem Cell 2010, 7:656-670.
67. Golachowska M.R., et al. MYO5B mutations in patients with microvillus inclusion disease presenting with transient renal Fanconi syndrome. J. Pediatr. Gastroenterol. Nutr. 2012, 54:491-498.
68. Thoeni C.E., et al. Microvillus inclusion disease: loss of Myosin vb disrupts intracellular traffic and cell polarity. Traffic 2014, 15:22-42.
69. Sigurbjörnsdóttir S., et al. Molecular mechanisms of de novo lumen formation. Nat. Rev. Mol. Cell Biol. 2014, 15:665-676.
70. Kamei M., et al. Endothelial tubes assemble from intracellular vacuoles in vivo. Nature 2006, 442:453-456.
71. Li D., et al. Kinesin-2 mediates apical endosome transport during epithelial lumen formation. Cell. Logist. 2014, 4:e28928.
72. Willenborg C., et al. Interaction between FIP5 and SNX18 regulates epithelial lumen formation. J. Cell Biol. 2011, 195:71-86.
73. Torkko J.M., et al. Depletion of apical transport proteins perturbs epithelial cyst formation and ciliogenesis. J. Cell Sci. 2008, 121:1193-1203.
74. Morais-de-Sá E., Sunkel C. Adherens junctions determine the apical position of the midbody during follicular epithelial cell division. EMBO Rep. 2013, 14:696-703.
75. Martin-Belmonte F., et al. PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42. Cell 2007, 128:383-397.
76. Field S.J., et al. PtdIns(4,5)P2 functions at the cleavage furrow during cytokinesis. Curr. Biol. 2005, 15:1407-1412.
77. Yu W., et al. Formation of cysts by alveolar type II cells in three-dimensional culture reveals a novel mechanism for epithelial morphogenesis. Mol. Biol. Cell 2007, 18:1693-1700.
78. Bedzhov I., Zernicka-Goetz M. Self-organizing properties of mouse pluripotent cells initiate morphogenesis upon implantation. Cell 2014, 156:1032-1044.
79. Zheng Z., et al. LGN regulates mitotic spindle orientation during epithelial morphogenesis. J. Cell Biol. 2010, 189:275-288.
80. Hao Y., et al. Par3 controls epithelial spindle orientation by aPKC-mediated phosphorylation of apical Pins. Curr. Biol. 2010, 20:1809-1818.
81. Rodriguez-Fraticelli A.E., et al. The Cdc42 GEF Intersectin 2 controls mitotic spindle orientation to form the lumen during epithelial morphogenesis. J. Cell Biol. 2010, 189:725-738.
82. Bañón-Rodríguez I., et al. EGFR controls IQGAP basolateral membrane localization, mitotic spindle orientation during epithelial morphogenesis. EMBO.J. 2014, 33:129-145.
83. Durgan J., et al. Par6B and atypical PKC regulate mitotic spindle orientation during epithelial morphogenesis. J. Biol. Chem. 2011, 286:12461-12474.
84. Monteleon C.L., D'Souza-Schorey C. Modeling disease using three dimensional cell culture: multi-lumen and inverted cyst phenotypes. Front. Biosci. 2012, 4:2864-2871.
85. Feracci H., et al. The establishment of hepatocyte cell surface polarity during fetal liver development. Dev. Biol. 1987, 123:73-84.
86. Fu D., et al. Coordinated elevation of mitochondrial oxidative phosphorylation and autophagy help drive hepatocyte polarization. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:7288-7293.
87. Fu D., et al. Increased mitochondrial fusion and autophagy help isolated hepatocytes repolarize in collagen sandwich cultures. Autophagy 2013, 9:2154-2155.
88. Bartles J.R., Hubbard A.L. Preservation of hepatocyte plasma membrane domains during cell division in situ in regenerating rat liver. Dev. Biol. 1986, 118:286-295.
89. Sato T., Clevers H. Growing self-organizing mini-guts from a single intestinal stem cell: mechanism and applications. Science 2013, 340:1190-1194.
90. Huch M., et al. Long-term culture of genome-stable bipotent stem cells from adult human liver. Cell 2015, 160:299-312.
91. Leung C.T., Brugge J.S. Outgrowth of single oncogene-expressing cells from suppressive epithelial environments. Nature 2012, 482:410-413.
92. Van Bergeijk P., et al. Optogenetic control of organelle transport and positioning. Nature 2015, 518:111-114.
93. Wartchow E.P., et al. Ciliary inclusion disease: report of a new primary ciliary dyskinesia variant. Pediatr. Dev. Pathol. 2014, 17:465-469.
94. Williams M.J., et al. Links between hepatic fibrosis, ductular reaction, and progenitor cell expansion. Gastroenterology 2014, 146:349-356.
95. Adams S.A., et al. Reversal of glandular polarity in the lymphovascular compartment of breast cancer. J. Clin. Pathol. 2004, 57:1114-1117.
96. Durdu S., et al. Luminal signalling links cell communication to tissue architecture during organogenesis. Nature 2014, 515:120-124.
97. Van der Velde K.J., et al. An overview and online registry of microvillus inclusion disease patients and their MYO5B mutations. Hum. Mutat. 2013, 34:1597-1605.
98. Saotome I., et al. Ezrin is essential for epithelial organization and villus morphogenesis in the developing intestine. Dev. Cell 2004, 6:855-864.
99. Whiteman E.L., et al. Crumbs3 is essential for proper epithelial development and viability. Mol. Cell. Biol. 2014, 34:43-56.
100. Knowles B.C., et al. Rab11a regulates Syntaxin 3 localization and microvillus assembly in enterocytes. J. Cell Sci. 2015, Published February 11, 2015. 10.1242/jcs.163303.
101. Sakamori R., et al. Cdc42 and Rab8a are critical for intestinal stem cell division, survival, and differentiation in mice. J. Clin. Invest. 2012, 122:1052-1065.
102. Melendez J., et al. Cdc42 coordinates proliferation, polarity, migration, and differentiation of small intestinal epithelial cells in mice. Gastroenterology 2013, 145:808-819.