β-pix directs collective migration of anterior visceral endoderm cells in the early mouse embryo

Genes and Development

Volumn 28, Issue 24, 2014, Pages 2764-2777

  Omelchenko, Tatiana ^a   Rabadan, M Angeles ^a   Hernáandez Martínez, Rocío ^a   Grego Bessa, Joaquim ^a   Anderson, Kathryn V ^a   Hall, Alan ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Anterior posterior axis; AVE migration; Collective cell migration; GEFs; Mouse embryo; Rho GTPases

Indexed keywords

RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; NEUROPEPTIDE; RAC1 PROTEIN, MOUSE; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTERIOR POSTERIOR AXIS; ANTERIOR VISCERAL ENDODERM CELL; ARTICLE; BETA PIX GENE; CELL JUNCTION; CELL MIGRATION; CELL MOTION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENDODERM; EPITHELIUM CELL; EXON; GENE; GENE DELETION; GENE EXPRESSION; GENE FREQUENCY; GENE FUNCTION; GENETIC CODE; GENOTYPE; HUMAN; HUMAN CELL; IN SITU HYBRIDIZATION; IN VITRO STUDY; INDEL MUTATION; KNOCKOUT MOUSE; LETHALITY; LIMIT OF QUANTITATION; MORPHOMETRICS; MOUSE; MOUSE EMBRYO; NONHUMAN; NUCLEOTIDE SEQUENCE; WESTERN BLOTTING; ANIMAL; ANIMAL EMBRYO; CYTOLOGY; GENETICS; METABOLISM; PROTEIN TRANSPORT; VISCERA;

MUS;

ANIMALS; CELL MOVEMENT; EMBRYO, MAMMALIAN; ENDODERM; EPITHELIAL CELLS; GENE DELETION; MICE; MICE, KNOCKOUT; NEUROPEPTIDES; PROTEIN TRANSPORT; RAC1 GTP-BINDING PROTEIN; RHO GUANINE NUCLEOTIDE EXCHANGE FACTORS; VISCERA;

EID: 84918582989     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.251371.114     Document Type: Article

References (48)

1. Andrew N, Insall RH. 2007. Chemotaxis in shallow gradients is mediated independently of PtdIns 3-kinase by biased choices between random protrusions. Nat Cell Biol 9: 193–200.
2. Arnold SJ, Robertson EJ. 2009. Making a commitment: cell lineage allocation and axis patterning in the early mouse embryo. Nat Rev Mol Cell Biol 10: 91–103.
3. Baird D, Feng Q, Cerione RA. 2006. Biochemical characterization of the Cool (cloned-out-of-library)/Pix (Pak-interactive exchange factor) proteins. Methods Enzymol 406: 58–69.
4. Bloomekatz J, Grego-Bessa J, Migeotte I, Anderson KV. 2012. Pten regulates collective cell migration during specification of the anterior-posterior axis of the mouse embryo. Dev Biol 364: 192–201.
5. Cau J, Hall A. 2005. Cdc42 controls the polarity of the actin and microtubule cytoskeletons through two distinct signal transduction pathways. J Cell Sci 118: 2579–2587.
6. Cherfils J, Zeghouf M. 2013. Regulation of small GTPases by GEFs, GAPs, and GDIs. Physiol Rev 93: 269–309.
7. Cheung KJ, Gabrielson E, Werb Z, Ewald AJ. 2013. Collective invasion in breast cancer requires a conserved basal epithelial program. Cell 155: 1639–1651.
8. Cozens AL, Yezzi MJ, Kunzelmann K, Ohrui T, Chin L, Eng K, Finkbeiner WE, Widdicombe JH, Gruenert DC. 1994. CFTR expression and chloride secretion in polarized immortal human bronchial epithelial cells. Am J Respir Cell Mol Biol 10: 38–47.
9. Eggenschwiler JT, Anderson KV. 2000. Dorsal and lateral fates in the mouse neural tube require the cell-autonomous activity of the open brain gene. Dev Biol 227: 648–660.
10. Fetisova EK, Ivanova OY, Potapova TV, Svitkina TM, Vasiliev JM. 1990. Competition of contacting heterotypic epithelial sheets for the territory in culture. Cell Biol Int Rep 14: 957– 965.
11. Friedl P, Gilmour D. 2009. Collective cell migration in morphogenesis, regeneration and cancer. Nat Rev Mol Cell Biol 10: 445–457.
12. Gloushankova NA, Krendel MF, Sirotkin VA, Bonder EM, Feder HH, Vasiliev JM, Gelfand IM. 1995. Dynamics of active lamellae in cultured epithelial cells: effects of expression of exogenous N-ras oncogene. Proc Natl Acad Sci 92: 5322– 5325.
13. Hayashi S, Lewis P, Pevny L, McMahon AP. 2002. Efficient gene modulation in mouse epiblast using a Sox2Cre transgenic mouse strain. Mech Dev 119: S97–S101.
14. Heasman SJ, Ridley AJ. 2008. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol 9: 690–701.
15. Hodgson L, Shen F, Hahn K. 2010. Biosensors for characterizing the dynamics of ρ family GTPases in living cells. Curr Protoc Cell Biol 46: 14.11.1–14.11.26.
16. Khalil AA, Friedl P. 2010. Determinants of leader cells in collective cell migration. Integr Biol (Camb) 2: 568–574.
17. Kim T, Park D. 2001. Molecular cloning and characterization of a novel mouse β-Pix isoform. Mol Cells 11: 89–94.
18. Kim S, Kim T, Lee D, Park SH, Kim H, Park D. 2000. Molecular cloning of neuronally expressed mouse β-Pix isoforms. Biochem Biophys Res Commun 272: 721–725.
19. Kimura-Yoshida C, Nakano H, Okamura D, Nakao K, Yonemura S, Belo JA, Aizawa S, Matsui Y, Matsuo I. 2005. Canonical Wnt signaling and its antagonist regulate anterior–posterior axis polarization by guiding cell migration in mouse visceral endoderm. Dev Cell 9: 639–650.
20. Kuo JC, Han X, Hsiao CT, Yates JR III, Waterman CM. 2011. Analysis of the myosin-II-responsive focal adhesion pro-teome reveals a role for β-Pix in negative regulation of focal adhesion maturation. Nat Cell Biol 13: 383–393.
21. Kutys ML, Yamada KM. 2014. An extracellular-matrix-specific GEF–GAP interaction regulates Rho GTPase crosstalk for 3D collagen migration. Nat Cell Biol 16: 909–917.
22. Machacek M, Hodgson L, Welch C, Elliott H, Pertz O, Nalbant P, Abell A, Johnson GL, Hahn K., Danuser G. 2009. Coordination of Rho GTPase activities during cell protrusion. Nature 461: 99–103.
23. Maretto S, Cordenonsi M, Dupont S, Braghetta P, Broccoli V, Hassan AB, Volpin D, Bressan GM, Piccolo S. 2003. Mapping Wnt/β-catenin signaling during mouse development and in colorectal tumors. Proc Natl Acad Sci 100: 3299–3304.
24. Migeotte I, Omelchenko T, Hall A, Anderson KV. 2010. Rac1-dependent collective cell migration is required for specification of the anterior–posterior body axis of the mouse. PLoS Biol 8: e1000442.
25. Morris SA, Grewal S, Barrios F, Patankar SN, Strauss B, Buttery L, Alexander M, Shakesheff KM, Zernicka-Goetz M. 2012. Dynamics of anterior–posterior axis formation in the developing mouse embryo. Nat Commun 3: 673.
26. Omelchenko T, Hall A. 2012. Myosin-IXA regulates collective epithelial cell migration by targeting RhoGAP activity to cell–cell junctions. Curr Biol 22: 278–288.
27. Omelchenko T, Vasiliev JM, Gelfand IM, Feder HH, Bonder EM. 2003. Rho-dependent formation of epithelial ‘leader’ cells during wound healing. Proc Natl Acad Sci 100: 10788– 10793.
28. Osmani N, Vitale N, Borg JP, Etienne-Manneville S. 2006. Scrib controls Cdc42 localization and activity to promote cell polarization during astrocyte migration. Curr Biol 16: 2395–2405.
29. Poujade M, Grasland-Mongrain E, Hertzog A, Jouanneau J, Chavrier P, Ladoux B, Buguin A, Silberzan P. 2007. Collective migration of an epithelial monolayer in response to a model wound. Proc Natl Acad Sci 104: 15988–15993.
30. Rakeman AS, Anderson KV. 2006. Axis specification and morphogenesis in the mouse embryo require Nap1, a regulator of WAVE-mediated actin branching. Development 133: 3075– 3083.
31. Rhee S, Yang SJ, Lee SJ, Park D. 2004. β-Pix-b(L), a novel isoform of β-Pix, is generated by alternative translation. Biochem Biophys Res Commun 318: 415–421.
32. Rhee JM, Pirity MK, Lackan CS, Long JZ, Kondoh G, Takeda J, Hadjantonakis AK. 2006. In vivo imaging and differential localization of lipid-modified GFP-variant fusions in embryonic stem cells and mice. Genesis 44: 202–218.
33. Rorth P. 2003. Communication by touch: role of cellular extensions in complex animals. Cell 112: 595–598.
34. Rorth P. 2007. Collective guidance of collective cell migration. Trends Cell Biol 17: 575–579.
35. Rorth P. 2011. Whence directionality: guidance mechanisms in solitary and collective cell migration. Dev Cell 20: 9–18.
36. Rossman KL, Der CJ, Sondek J. 2005. GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat Rev Mol Cell Biol 6: 167–180.
37. Skarnes WC, Rosen B, West AP, Koutsourakis M, Bushell W, Iyer V, Mujica AO, Thomas M, Harrow J, Cox T, et al. 2011. A conditional knockout resource for the genome-wide study of mouse gene function. Nature 474: 337–342.
38. Srinivas S, Rodriguez T, Clements M, Smith JC, Beddington RS. 2004. Active cell migration drives the unilateral movements of the anterior visceral endoderm. Development 131: 1157– 1164.
39. Takaoka K, Hamada H. 2012. Cell fate decisions and axis determination in the early mouse embryo. Development 139: 3–14.
40. Takaoka K, Yamamoto M, Hamada H. 2011. Origin and role of distal visceral endoderm, a group of cells that determines anterior-posterior polarity of the mouse embryo. Nat Cell Biol 13: 743–752.
41. Tatin F, Taddei A, Weston A, Fuchs E, Devenport D, Tissir F, Makinen T. 2013. Planar cell polarity protein Celsr1 regulates endothelial adherens junctions and directed cell rearrangements during valve morphogenesis. Dev Cell 26: 31–44.
42. ten Klooster JP, Jaffer ZM, Chernoff J, Hordijk PL. 2006. Targeting and activation of Rac1 are mediated by the exchange factor β-Pix. J Cell Biol 172: 759–769.
43. Trichas G, Joyce B, Crompton LA, Wilkins V, Clements M, Tada M, Rodriguez TA, Srinivas S. 2011. Nodal dependent differential localisation of dishevelled-2 demarcates regions of differing cell behaviour in the visceral endoderm. PLoS Biol 9: e1001019.
44. Trichas G, Smith AM, White N, Wilkins V, Watanabe T, Moore A, Joyce B, Sugnaseelan J, Rodriguez TA, Kay D, et al. 2012. Multi-cellular rosettes in the mouse visceral endoderm facilitate the ordered migration of anterior visceral endoderm cells. PLoS Biol 10: e1001256.
45. Vedula SR, Leong MC, Lai TL, Hersen P, Kabla AJ, Lim CT, Ladoux B. 2012. Emerging modes of collective cell migration induced by geometrical constraints. Proc Natl Acad Sci 109: 12974–12979.
46. Xu X, Jin D, Durgan J, Hall A. 2013. LKB1 controls human bronchial epithelial morphogenesis through p114RhoGEF-dependent RhoA activation. Mol Cell Biol 33: 2671–2682.
47. Yamamoto M, Saijoh Y, Perea-Gomez A, Shawlot W, Behringer RR, Ang SL, Hamada H, Meno C. 2004. Nodal antagonists regulate formation of the anteroposterior axis of the mouse embryo. Nature 428: 387–392.
48. Yoshizawa M, Sone M, Matsuo N, Nagase T, Ohara O, Nabeshima Y, Hoshino M. 2003. Dynamic and coordinated expression profile of dbl-family guanine nucleotide exchange factors in the developing mouse brain. Gene Expr Patterns 3: 375–381.