Cellular and molecular mechanisms of single and collective cell migrations in drosophila: Themes and variations

Annual Review of Genetics

Volumn 48, Issue , 2014, Pages 295-318

  Pocha, Shirin M ^a   Montell, Denise J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

chemotaxis; development; EMT; tubulogenesis

Indexed keywords

FIBROBLAST GROWTH FACTOR; JANUS KINASE; MYOSIN; NETRIN; PROTEIN TYROSINE KINASE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; STAT PROTEIN; UVOMORULIN;

ARTICLE; BLOOD CELL; CELL ADHESION; CELL MATURATION; CELL MIGRATION; CELL MOTILITY; CELL MOTION; CELL SHAPE; CHEMICAL MODIFICATION; CHEMOTAXIS; DISEASES; DROSOPHILA; EPITHELIAL MESENCHYMAL TRANSITION; GASTRULATION; GENETICS; MOLECULAR MECHANICS; NONHUMAN; POLARIZATION; PRIMORDIAL GERM CELL; SALIVARY GLAND; SIGNAL TRANSDUCTION; TRACHEA; WOUND; ANIMAL; CYTOSKELETON; GROWTH, DEVELOPMENT AND AGING; HUMAN; MORPHOGENESIS;

ANIMALS; CELL MOVEMENT; CYTOSKELETON; DROSOPHILA; HUMANS; MORPHOGENESIS; SIGNAL TRANSDUCTION;

EID: 84913525095     PISSN: 00664197     EISSN: 15452948     Source Type: Book Series    
DOI: 10.1146/annurev-genet-120213-092218     Document Type: Article

References (144)

1. Abercrombie M, Heaysman JEM. 1953. Observations on the social behaviour of cells in tissue culture. I. Speed of movement of chick heart fibroblasts in relation to their mutual contacts. Exp. Cell Res. 5:111-31
2. Badolato R. 2013. Defects of leukocyte migration in primary immunodeficiencies. Eur. J. Immunol. 43:1436-40
3. Bai J, Uehara Y, Montell DJ. 2000. Regulation of invasive cell behavior by taiman, a Drosophila protein related to AIB1, a steroid receptor coactivator amplified in breast cancer. Cell 103:1047-58
4. Barrett K, Leptin M, Settleman J. 1997. The Rho GTPase and a putative RhoGEF mediate a signaling pathway for the cell shape changes in Drosophila gastrulation. Cell 91:905-15
5. Bastock R, Strutt D. 2007. The planar polarity pathway promotes coordinated cell migration during Drosophila oogenesis. Development 134:3055-64
6. Baum B, Settleman J, Quinlan MP. 2008. Transitions between epithelial and mesenchymal states in development and disease. Semin. Cell Dev. Biol. 19:294-308
7. Bement WM, Forscher P, Mooseker MS. 1993. A novel cytoskeletal structure involved in purse string wound closure and cell polarity maintenance. J. Cell Biol. 121:565-78
8. Borghese L, Fletcher G, Mathieu J, Atzberger A, Eades WC, et al. 2006. Systematic analysis of the transcriptional switch inducing migration of border cells. Dev. Cell 10:497-508
9. Bradford D, Cole SJ, Cooper HM. 2009. Netrin-1: diversity in development. Int. J. Biochem. Cell Biol. 41:487-93
10. Bradley PL, Andrew DJ. 2001. Ribbon encodes a novel BTB/POZ protein required for directed cell migration in Drosophila melanogaster. Development 128:3001-15
11. Bradley PL, Haberman AS, Andrew DJ. 2001. Organ formation in Drosophila: specification and morphogenesis of the salivary gland. BioEssays 23:901-11
12. Bradley PL, Myat MM, Comeaux CA, Andrew DJ. 2003. Posterior migration of the salivary gland requires an intact visceral mesoderm and integrin function. Dev. Biol. 257:249-62
13. Bruckner K, Kockel L, Duchek P, Luque CM, Rorth P, Perrimon N. 2004. The PDGF/VEGF receptor controls blood cell survival in Drosophila. Dev. Cell 7:73-84
14. Burnett C, Howard K. 2003. Fly and mammalian lipid phosphate phosphatase isoforms differ in activity both in vitro and in vivo. EMBO Rep. 4:793-99
15. Cai D, Chen SC, Prasad M, He L, Wang X, et al. 2014. Mechanical feedback through E-Cadherin promotes direction sensing during collective cell migration. Cell 157:1143-59
16. Caussinus E, Colombelli J, Affolter M. 2008. Tip-cell migration controls stalk-cell intercalation during Drosophila tracheal tube elongation. Curr. Biol. 18:1727-34
17. Chanet S, Schweisguth F. 2012. Regulation of epithelial polarity by the E3 ubiquitin ligase Neuralized and the Bearded inhibitors in Drosophila. Nat. Cell Biol. 14:467-76
18. Chen LY, Pan ZK. 2009. Synergistic activation of leukocytes by bacterial chemoattractants: potential drug targets. Endocr. Metab. Immune Disord. Drug Targets 9:361-70
19. Cheshire AM, Kerman BE, Zipfel WR, Spector AA, Andrew DJ. 2008. Kinetic and mechanical analysis of live tube morphogenesis. Dev. Dyn. 237:2874-88
20. Chihara T, Kato K, Taniguchi M, Ng J, Hayashi S. 2003. Rac promotes epithelial cell rearrangement during tracheal tubulogenesis in Drosophila. Development 130:1419-28
21. Cho NK, Keyes L, Johnson E, Heller J, Ryner L, et al. 2002. Developmental control of blood cell migration by the Drosophila VEGF Pathway. Cell 108:865-76
22. Choi W, Harris NJ, Sumigray KD, Peifer M. 2013. Rap1 andCanoe/afadin are essential for establishment of apical-basal polarity in the Drosophila embryo. Mol. Biol. Cell 24:945-63
23. Davis JR, Huang C-Y, Zanet J, Harrison S, Rosten E, et al. 2012. Emergence of embryonic pattern through contact inhibition of locomotion. Development 139:4555-60
24. DeGennaro M, Hurd TR, Siekhaus DE, Biteau B, Jasper H, Lehmann R. 2011. Peroxiredoxin stabilization of DE-Cadherin promotes primordial germ cell adhesion. Dev. Cell 20:233-43
25. Deshpande G, Zhou K, Wan JY, Friedrich J, Jourjine N, et al. 2013. The hedgehog pathway gene shifted functions together with the hmgcr-dependent isoprenoid biosynthetic pathway to orchestrate germ cell migration. PLOS Genet. 9:e1003720
26. Di Gennaro A, Haeggstrom JZ. 2012. The leukotrienes: immune-modulating lipid mediators of disease. Adv. Immunol. 116:51-92
27. Duchek P, Rorth P. 2001. Guidance of cell migration by EGF receptor signaling during Drosophila oogenesis. Science 291:131-33
28. Duchek P, Somogyi K, Jekely G, Beccari S, Rorth P. 2001. Guidance of cell migration by the Drosophila PDGF/VEGF receptor. Cell 107:17-26
29. Dumartin L, Quemener C, Laklai H, Herbert J, Bicknell R, et al. 2010. Netrin-1 mediates early events in pancreatic adenocarcinoma progression, acting on tumor and endothelial cells. Gastroenterology 138:1595-606
30. Engelhardt B, Ransohoff RM. 2012. Capture, crawl, cross: the T cell code to breach the blood-brain barriers. Trends Immunol. 33:579-89
31. Englund C, Steneberg P, Falileeva L, Xylourgidis N, Samakovlis C. 2002. Attractive and repulsive functions of Slit are mediated by different receptors in the Drosophila trachea. Development 129:4941-51
32. Frasch M. 1995. Induction of visceral and cardiac mesoderm by ectodermal Dpp in the early Drosophila embryo. Nature 374:464-67
33. Fulga TA, Rorth P. 2002. Invasive cell migration is initiated by guided growth of long cellular extensions. Nat. Cell Biol. 4:715-19
34. Gates J, Mahaffey JP, Rogers SL, Emerson M, Rogers EM, et al. 2007. Enabled plays key roles in embryonic epithelial morphogenesis in Drosophila. Development 134:2027-39
35. Ghabrial A, Luschnig S, Metzstein MM, Krasnow MA. 2003. Branchingmorphogenesis of the Drosophila tracheal system. Annu. Rev. Cell Dev. Biol. 19:623-47
36. Ghabrial AS, Krasnow MA. 2006. Social interactions among epithelial cells during tracheal branching morphogenesis. Nature 441:746-49
37. Gheldof A, Berx G. 2013. Cadherins and epithelial-to-mesenchymal transition. Prog. Mol. Biol. Transl. Sci. 116:317-36
38. Ghysen A, Dambly-Chaudiere C. 2004. Development of the zebrafish lateral line. Curr. Opin. Neurobiol. 14:67-73
39. Gorfinkiel N, Arias AM. 2007. Requirements for adherens junction components in the interaction between epithelial tissues during dorsal closure in Drosophila. J. Cell Sci. 120:3289-98
40. Grosshans J, Wieschaus E. 2000. A genetic link between morphogenesis and cell division during formation of the ventral furrow in Drosophila. Cell 101:523-31
41. Haas P, Gilmour D. 2006. Chemokine signalingmediates self-organizing tissuemigration in the zebrafish lateral line. Dev. Cell 10:673-80
42. Hacker U, Perrimon N. 1998. DRhoGEF2 encodes a member of the Dbl family of oncogenes and controls cell shape changes during gastrulation in Drosophila. Genes Dev. 12:274-84
43. Hall A. 2012. Rho family GTPases. Biochem. Soc. Trans. 40:1378-82
44. Hanyu-Nakamura K, Kobayashi S, Nakamura A. 2004. Germ cell-Autonomous Wunen2 is required for germline development in Drosophila embryos. Development 131:4545-53
45. Harris KE, Beckendorf SK. 2007. Different Wnt signals act through the Frizzled and RYK receptors during Drosophila salivary gland migration. Development 134:2017-25
46. Hobson RP. 1935. On a fat-soluble growth factor required by blow-fly larvae: identity of the growth factor with cholesterol. Biochem. J. 29:2023-26
47. Hsouna A, Nallamothu G, Kose N, Guinea M, Dammai V, Hsu T. 2010. Drosophila von Hippel-Lindau tumor suppressor gene function in epithelial tubule morphogenesis. Mol. Cell. Biol. 30:3779-94
48. Ikeya T, Hayashi S. 1999. Interplay of Notch and FGF signaling restricts cell fate and MAPK activation in the Drosophila trachea. Development 126:4455-63
49. Iwai Y, Usui T, Hirano S, Steward R, Takeichi M, Uemura T. 1997. Axon patterning requires DNcadherin, a novel neuronal adhesion receptor, in the Drosophila embryonic CNS. Neuron 19:77-89
50. Jacinto A, Wood W, Balayo T, Turmaine M, Martinez-Arias A, Martin P. 2000 . Dynamic actin-based epithelial adhesion and cell matching during Drosophila dorsal closure. Curr. Biol. 10:1420-26
51. Jaglarz MK, Howard KR. 1995. The active migration of Drosophila primordial germ cells. Development 121:3495-503
52. Jang AC, Chang YC, Bai J, Montell D. 2009. Border-cell migration requires integration of spatial and temporal signals by the BTB protein Abrupt. Nat. Cell Biol. 11:569-79
53. Jankovics F, Brunner D. 2006. Transiently reorganized microtubules are essential for zippering during dorsal closure in Drosophila melanogaster. Dev. Cell 11:375-85
54. Janssens K, Sung HH, Rorth P. 2010. Direct detection of guidance receptor activity during border cell migration. Proc. Natl. Acad. Sci. USA 107:7323-28
55. Kaltschmidt JA, Lawrence N, Morel V, Balayo T, Fernandez BG, et al. 2002. Planar polarity and actin dynamics in the epidermis of Drosophila. Nat. Cell Biol. 4:937-44
56. Kawauchi T, Shikanai M, Kosodo Y. 2013. Extra-cell cycle regulatory functions of cyclin-dependent kinases (CDK) and CDK inhibitor proteins contribute to brain development and neurological disorders. Genes Cells 18:176-94
57. Kerman BE, Cheshire AM, Myat MM, Andrew DJ. 2008. Ribbon modulates apical membrane during tube elongation through Crumbs and Moesin. Dev. Biol. 320:278-88
58. Kiehart DP, Galbraith CG, Edwards KA, Rickoll WL, Montague RA. 2000. Multiple forces contribute to cell sheet morphogenesis for dorsal closure in Drosophila. J. Cell Biol. 149:471-90
59. Killeen MT, Sybingco SS. 2008. Netrin, Slit, and Wnt receptors allow axons to choose the axis of migration. Dev. Biol. 323:143-51
60. Kolesnikov T, Beckendorf SK. 2005. NETRIN and SLIT guide salivary gland migration. Dev. Biol. 284:102-11
61. Kollmar R, Nakamura SK, Kappler JA, Hudspeth AJ. 2001. Expression and phylogeny of claudins in vertebrate primordia. Proc. Natl. Acad. Sci. USA 98:10196-201
62. Kunwar PS, Sano H, Renault AD, Barbosa V, Fuse N, Lehmann R. 2008. Tre1 GPCR initiates germ cell transepithelial migration by regulating Drosophila melanogaster E-Cadherin. J. Cell Biol. 183:157-68
63. Kunwar PS, Starz-Gaiano M, Bainton RJ, Heberlein U, Lehmann R. 2003. Tre1, a G protein-coupled receptor, directs transepithelial migration of Drosophila germ cells. PLOS Biol. 1:E80
64. Laplante C, Nilson LA. 2011. Asymmetric distribution of Echinoid defines the epidermal leading edge during Drosophila dorsal closure. J. Cell Biol. 192:335-48
65. Lauffenburger DA, Horwitz AF. 1996. Cell migration: a physically integrated molecular process. Cell 84:359-69
66. Lebreton G, Casanova J. 2014. Specification of leading and trailing cell features during collective migration in the Drosophila trachea. J. Cell Sci. 127:465-74
67. Leptin M, Grunewald B. 1990. Cell shape changes during gastrulation in Drosophila. Development 110:73-84
68. Leptin M, Roth S. 1994. Autonomy and non-Autonomy in Drosophila mesoderm determination and morphogenesis. Development 120:853-59
69. Levayer R, Lecuit T. 2013. Oscillation and polarity of E-Cadherin asymmetries control actomyosin flow patterns during morphogenesis. Dev. Cell 26:162-75
70. Liu R, Woolner S, Johndrow JE, Metzger D, Flores A, Parkhurst SM. 2008. Sisyphus, the Drosophila myosin XV homolog, traffics within filopodia transporting key sensory and adhesion cargos. Development 135:53-63
71. Llense F, Martin-Blanco E. 2008. JNK signaling controls border cell cluster integrity and collective cell migration. Curr. Biol. 18:538-44
72. Magie CR, Meyer MR, Gorsuch MS, Parkhurst SM. 1999. Mutations in the Rho1 small GTPase disrupt morphogenesis and segmentation during early Drosophila development. Development 126:5353-64
73. Majumder P, Aranjuez G, Amick J, McDonald JA. 2012. Par-1 controls myosin-II activity through myosin phosphatase to regulate border cell migration. Curr. Biol. 22:363-72
74. Martin AC, Kaschube M, Wieschaus EF. 2009. Pulsed contractions of an actin-myosin network drive apical constriction. Nature 457:495-99
75. McDonald JA, Khodyakova A, Aranjuez G, Dudley C, Montell DJ. 2008. PAR-1 kinase regulates epithelial detachment and directional protrusion of migrating border cells. Curr. Biol. 18:1659-67
76. McDonald JA, Pinheiro EM, Kadlec L, Schupbach T, Montell DJ. 2006. Multiple EGFR ligands participate in guiding migrating border cells. Dev. Biol. 296:94-103
77. McDonald JA, Pinheiro EM, Montell DJ. 2003. PVF1, a PDGF/VEGF homolog, is sufficient to guide border cells and interacts genetically with Taiman. Development 130:3469-78
78. McGregor JR, Xi R, Harrison DA. 2002. JAK signaling is somatically required for follicle cell differentiation in Drosophila. Development 129:705-17
79. McMahon A, Supatto W, Fraser SE, Stathopoulos A. 2008. Dynamic analyses of Drosophila gastrulation provide insights into collective cell migration. Science 322:1546-50
80. Mehlen P, Delloye-Bourgeois C, Chedotal A. 2011. Novel roles for Slits and netrins: axon guidance cues as anticancer targets? Nat. Rev. Cancer 11:188-97
81. Millard TH, Martin P. 2008. Dynamic analysis of filopodial interactions during the zippering phase of Drosophila dorsal closure. Development 135:621-26
82. Monahan AJ, Starz-Gaiano M. 2013. Socs36E attenuates STAT signaling to optimize motile cell specification in the Drosophila ovary. Dev. Biol. 379:152-66
83. Montell DJ, Yoon WH, Starz-Gaiano M. 2012. Group choreography: mechanisms orchestrating the collective movement of border cells. Nat. Rev. Mol. Cell Biol. 13:631-45
84. Moreira S, Stramer B, Evans I, Wood W, Martin P. 2010. Prioritization of competing damage and developmental signals by migrating macrophages in the Drosophila embryo. Curr. Biol. 20:464-70
85. Morel V, Arias AM. 2004. Armadillo/β-Catenin-dependent Wnt signalling is required for the polarisation of epidermal cells during dorsal closure in Drosophila. Development 131:3273-83
86. Murphy AM, Montell DJ. 1996. Cell type-specific roles for Cdc42, Rac, and RhoL in Drosophila oogenesis. J. Cell Biol. 133:617-30
87. Murray MJ, Saint R. 2007. Photoactivatable GFP resolves Drosophila mesoderm migration behaviour. Development 134:3975-83
88. Myat MM, Andrew DJ. 2000. Organ shape in the Drosophila salivary gland is controlled by regulated, sequential internalization of the primordia. Development 127:679-91
89. Niewiadomska P, Godt D, Tepass U. 1999. DE-Cadherin is required for intercellular motility during Drosophila oogenesis. J. Cell Biol. 144:533-47
90. Norman MU, Hickey MJ. 2005. Mechanisms of lymphocyte migration in autoimmune disease. Tissue Antigens 66:163-72
91. Oda H, Tsukita S, Takeichi M. 1998. Dynamic behavior of the cadherin-based cell-cell adhesion system during Drosophila gastrulation. Dev. Biol. 203:435-50
92. Parsons B, Foley E. 2013. The Drosophila platelet-derived growth factor and vascular endothelial growth factor-receptor related (Pvr) protein ligands Pvf2 and Pvf3 control hemocyte viability and invasive migration. J. Biol. Chem. 288:20173-83
93. Peinado H, Ballestar E, Esteller M, Cano A. 2004. Snail mediates E-Cadherin repression by the recruitment of the Sin3A/histone deacetylase 1 (HDAC1)/HDAC2 complex. Mol. Cell. Biol. 24:306-19
94. Pinheiro EM, Montell DJ. 2004. Requirement for Par-6 and Bazooka in Drosophila border cellmigration. Development 131:5243-51
95. Pirraglia C, Jattani R, Myat MM. 2006. Rac function in epithelial tube morphogenesis. Dev. Biol. 290:435-46
96. Pirraglia C, Walters J, Ahn N, Myat MM. 2013. Rac1 GTPase acts downstream of αPS1βPS integrin to control collective migration and lumen size in the Drosophila salivary gland. Dev. Biol. 377:21-32
97. Poukkula M, Cliffe A, Changede R, Rorth P. 2011. Cell behaviors regulated by guidance cues in collective migration of border cells. J. Cell Biol. 192:513-24
98. Prasad M, Montell DJ. 2007. Cellular andmolecular mechanisms of border cellmigration analyzed using time-lapse live-cell imaging. Dev. Cell 12:997-1005
99. Ramel D, Wang X, Laflamme C, Montell DJ, Emery G. 2013. Rab11 regulates cell-cell communication during collective cell movements. Nat. Cell Biol. 15:317-24
100. Rauzi M, Lenne PF, Lecuit T. 2010. Planar polarized actomyosin contractile flows control epithelial junction remodelling. Nature 468:1110-14
101. Renault AD, Kunwar PS, Lehmann R. 2010. Lipid phosphate phosphatase activity regulates dispersal and bilateral sorting of embryonic germ cells in Drosophila. Development 137:1815-23
102. Renault AD, Sigal YJ, Morris AJ, Lehmann R. 2004. Soma-germ line competition for lipid phosphate uptake regulates germ cell migration and survival. Science 305:1963-66
103. Ricardo S, Lehmann R. 2009. An ABC transporter controls export of a Drosophila germ cell attractant. Science 323:943-46
104. Richardson BE, Lehmann R. 2010. Mechanisms guiding primordial germ cell migration: strategies from different organisms. Nat. Rev. Mol. Cell Biol. 11:37-49
105. Ring JM, Martinez Arias A. 1993. Puckered, a gene involved in position-specific cell differentiation in the dorsal epidermis of the Drosophila larva. Development 19(Suppl.):251-59
106. Samakovlis C, Hacohen N, Manning G, Sutherland DC, Guillemin K, Krasnow MA. 1996. Development of the Drosophila tracheal system occurs by a series of morphologically distinct but genetically coupled branching events. Development 122:1395-407
107. Sano H, Renault AD, Lehmann R. 2005. Control of lateral migration and germ cell elimination by the Drosophila melanogaster lipid phosphate phosphatasesWunen andWunen. J. Cell Biol. 171:675-83
108. Santos AC, Lehmann R. 2004. Isoprenoids control germ cell migration downstream of HMGCoA reductase. Dev. Cell 6:283-93
109. Schäfer G, Narasimha M, Vogelsang E, Leptin M. 2014. Cadherin switching during the formation and differentiation of the Drosophila mesoderm: implications for epithelial mesenchymal transitions. J. Cell Sci. 127:1511-22
110. Seher TC, Narasimha M, Vogelsang E, Leptin M. 2007. Analysis and reconstitution of the genetic cascade controlling early mesoderm morphogenesis in the Drosophila embryo. Mech. Dev. 124:167-79
111. Seifert JR, Lehmann R. 2012. Drosophila primordial germ cell migration requires epithelial remodeling of the endoderm. Development 139:2101-6
112. Shamir ER, Pappalardo E, Jorgens DM, Coutinho K, Tsai WT, et al. 2014. Twist1-induced dissemination preserves epithelial identity and requires E-Cadherin. J. Cell Biol. 204:839-56
113. Shishido E, Higashijima S, Emori Y, Saigo K. 1993. Two FGF-receptor homologues of Drosophila: one is expressed in mesodermal primordium in early embryos. Development 117:751-61
114. Silver DL, Montell DJ. 2001. Paracrine signaling through the JAK/STAT pathway activates invasive behavior of ovarian epithelial cells in Drosophila. Cell 107:831-41
115. Smallhorn M, Murray MJ, Saint R. 2004. The epithelial-mesenchymal transition of the Drosophila mesoderm requires the Rho GTP exchange factor Pebble. Development 131:2641-51
116. Solon J, Kaya-Copur A, Colombelli J, Brunner D. 2009. Pulsed forces timed by a ratchet-likemechanism drive directed tissue movement during dorsal closure. Cell 137:1331-42
117. Spahn P, Ott A, Reuter R. 2012. The PDZ-GEF protein Dizzy regulates the establishment of adherens junctions required for ventral furrow formation in Drosophila. J. Cell Sci. 125:3801-12
118. Starz-Gaiano M, Cho NK, Forbes A, Lehmann R. 2001. Spatially restricted activity of a Drosophila lipid phosphatase guides migrating germ cells. Development 128:983-91
119. Starz-Gaiano M, Melani M, Meinhardt H, Montell D. 2009. Interpretation of the UPD/JAK/STAT morphogen gradient in Drosophila follicle cells. Cell Cycle 8:2917-25
120. Starz-Gaiano M, Melani M, Wang X, Meinhardt H, Montell DJ. 2008. Feedback inhibition of Jak/STAT signaling by apontic is required to limit an invasive cell population. Dev. Cell 14:726-38
121. Stathopoulos A, Tam B, Ronshaugen M, Frasch M, Levine M. 2004. Pyramus and thisbe: FGF genes that pattern the mesoderm of Drosophila embryos. Genes Dev. 18:687-99
122. Stathopoulos A, Van Drenth M, Erives A, Markstein M, Levine M. 2002. Whole-genome analysis of dorsal-ventral patterning in the Drosophila embryo. Cell 111:687-701
123. Stramer B, Moreira S, Millard T, Evans I, Huang C-Y, et al. 2010. Clasp-mediated microtubule bundling regulates persistent motility and contact repulsion in Drosophila macrophages in vivo. J. Cell Biol. 189:681-89
124. Stramer B, Wood W, Galko MJ, Redd MJ, Jacinto A, et al. 2005. Live imaging of wound inflammation in Drosophila embryos reveals key roles for small GTPases during in vivo cell migration. J. Cell Biol. 168:567-73
125. Sutherland D, Samakovlis C, Krasnow MA. 1996. Branchless encodes a Drosophila FGF homolog that controls tracheal cell migration and the pattern of branching. Cell 87:1091-101
126. Takahashi Y, Sipp D, Enomoto H. 2013. Tissue interactions in neural crest cell development and disease. Science 341:860-63
127. Tepass U, Fessler LI, Aziz A, Hartenstein V. 1994. Embryonic origin of hemocytes and their relationship to cell death in Drosophila. Development 120:1829-37
128. Theveneau E, Steventon B, Scarpa E, Garcia S, Trepat X, et al. 2013. Chase-And-run between adjacent cell populations promotes directional collective migration. Nat. Cell Biol. 15:763-72
129. Tulin S, Stathopoulos A. 2010. Analysis of Thisbe and Pyramus functional domains reveals evidence for cleavage of Drosophila FGFs. BMC Dev. Biol. 10:83
130. Van Doren M, Broihier HT, Moore LA, Lehmann R. 1998. HMG-CoA reductase guides migrating primordial germ cells. Nature 396:466-69
131. Vincent Sp, Wilson R, Coelho C, Affolter M, Leptin M. 1998. The Drosophila protein Dof is specifically required for FGF signaling. Mol. Cell 2:515-25
132. Wang X, Adam JC, Montell D. 2007. Spatially localized Kuzbanian required for specific activation of Notch during border cell migration. Dev. Biol. 301:532-40
133. Wang X, Bo J, Bridges T, Dugan KD, Pan TC, et al. 2006. Analysis of cellmigration usingwhole-genome expression profiling of migratory cells in the Drosophila ovary. Dev. Cell 10:483-95
134. Wang X, He L, Wu YI, Hahn KM, Montell DJ. 2010. Light-mediated activation reveals a key role for Rac in collective guidance of cell movement in vivo. Nat. Cell Biol. 12:591-97
135. Wells A, Grahovac J, Wheeler S, Ma B, Lauffenburger D. 2013. Targeting tumor cell motility as a strategy against invasion and metastasis. Trends Pharmacol. Sci. 34:283-89
136. Werbowetski-Ogilvie TE, Seyed Sadr M, Jabado N, Angers-Loustau A, Agar NY, et al. 2006. Inhibition of medulloblastoma cell invasion by Slit. Oncogene 25:5103-12
137. Woolner S, Jacinto A, Martin P. 2005. The small GTPase Rac plays multiple roles in epithelial sheet fusion: dynamic studies of Drosophila dorsal closure. Dev. Biol. 282:163-73
138. Xu F, Zhang C, Graves DT. 2013. Abnormal cell responses and role of TNF-α in impaired diabetic wound healing. BioMed Res. Int. 2013:754802
139. Xu N, Keung B, Myat MM. 2008. Rho GTPase controls invagination and cohesive migration of the Drosophila salivary gland through Crumbs and Rho-kinase. Dev. Biol. 321:88-100
140. Yang J, Weinberg RA. 2008. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell 14:818-29
141. Yoon WH, Meinhardt H, Montell DJ. 2011. MiRNA-mediated feedback inhibition of JAK/STAT morphogen signalling establishes a cell fate threshold. Nat. Cell Biol. 13:1062-69
142. Young PE, Richman AM, Ketchum AS, Kiehart DP. 1993. Morphogenesis in Drosophila requires nonmuscle myosin heavy chain function. Genes Dev. 7:29-41
143. Zhang N, Zhang J, Cheng Y, Howard K. 1996. Identification and genetic analysis of wunen, a gene guiding Drosophila melanogaster germ cell migration. Genetics 143:1231-41
144. Zhang N, Zhang J, Purcell KJ, Cheng Y, Howard K. 1997. The Drosophila protein Wunen repels migrating germ cells. Nature 385:64-67