Abelson kinase acts as a robust, multifunctional scaffold in regulating embryonic morphogenesis

Molecular Biology of the Cell

Volumn 27, Issue 16, 2016, Pages 2613-2631

  Rogers, Edward M ^a   Spracklen, Andrew J ^a   Bilancia, Colleen G ^a   Sumigray, Kaelyn D ^a   Allred, S Colby ^a   Nowotarski, Stephanie H ^a   Schaefer, Kristina N ^a   Ritchie, Benjamin J ^a   Peifer, Mark ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABELSON KINASE; ACTIN; ACTIN BINDING PROTEIN; SCAFFOLD PROTEIN; DROSOPHILA PROTEIN; PROTEIN BINDING;

ACTIN FILAMENT; ARTICLE; CELL FUNCTION; CELL SHAPE; CELL VIABILITY; CYTOSKELETON; DROSOPHILA; EMBRYO DEVELOPMENT; MESODERM; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF; TRANSGENE; ANIMAL; DROSOPHILA MELANOGASTER; EMBRYOLOGY; GENETICS; METABOLISM; ONCOGENE; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAIN;

ACTINS; AMINO ACID MOTIFS; ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYONIC DEVELOPMENT; GENES, ABL; MORPHOGENESIS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN DOMAINS; PROTO-ONCOGENE PROTEINS C-ABL; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAINS;

EID: 84982106460     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E16-05-0292     Document Type: Article

References (78)

1. Ahern-Djamali SM, Bachmann C, Hua P, Reddy SK, Kastenmeier AS, Walter U, Hoffmann FM (1999). Identification of profilin and src homology 3 domains as binding partners for Drosophila enabled. Proc Natl Acad Sci USA 96, 4977-4982.
2. Antoku S, Saksela K, Rivera GM, Mayer BJ (2008). A crucial role in cell spreading for the interaction of Abl PxxP motifs with Crk and Nck adaptors. J Cell Sci 121, 3071-3082.
3. Bell ES, Park M (2012). Models of crk adaptor proteins in cancer. Genes Cancer 3, 341-352.
4. Bischof J, Maeda RK, Hediger M, Karch F, Basler K (2007). An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc Natl Acad Sci USA 104, 3312-3317.
5. Bradley WD, Hernandez SE, Settleman J, Koleske AJ (2006). Integrin signaling through Arg activates p190RhoGAP by promoting its binding to p120RasGAP and recruitment to the membrane. Mol Biol Cell 17, 4827-4836.
6. Bradley WD, Koleske AJ (2009). Regulation of cell migration and morphogenesis by Abl-family kinases: emerging mechanisms and physiological contexts. J Cell Sci 122, 3441-3454.
7. Chou T-B, Noll E, Perrimon N (1993). Autosomal P[ovoD1] dominant female-sterile insertions in Drosophila and their use in generating female germ-line chimeras. Development 119, 1359-1369.
8. Chou TB, Perrimon N (1996). The autosomal FLP-DFS technique for generating germline mosaics in Drosophila melanogaster. Genetics 144, 1673-1679.
9. Clarkson M, Saint R (1999). A His2AvDGFP fusion gene complements a lethal His2AvD mutant allele and provides an in vivo marker for Drosophila chromosome behavior. DNA Cell Biol 18, 457-462.
10. Comer AR, Ahern-Djamali SM, Juang J-L, Jackson PD, Hoffmann FM (1998). Phosphorylation of Enabled by the Drosophila Abelson tyrosine kinase regulates the in vivo function and protein-protein interactions of Enabled. Mol Cell Biol 18, 152-160.
11. Courtemanche N, Gifford SM, Simpson MA, Pollard TD, Koleske AJ (2015). Abl2/Abl-related gene stabilizes actin filaments, stimulates actin branching by actin-related protein 2/3 complex, and promotes actin filament severing by cofilin. J Biol Chem 290, 4038-4046.
12. Desai CJ, Garrity PA, Keshishian H, Zipursky SL, Zinn K (1999). The Drosophila SH2-SH3 adapter protein Dock is expressed in embryonic axons and facilitates synapse formation by the RP3 motoneuron. Development 126, 1527-1535.
13. Druker BJ (2008). Translation of the Philadelphia chromosome into therapy for CML. Blood 112, 4808-4817.
14. Edwards KA, Demsky M, Montague RA, Weymouth N, Kiehart DP (1997). GFP-moesin illuminates actin cytoskeleton dynamics in living tissue and demonstrates cell shape changes during morphogenesis in Drosophila. Dev Biol 191, 103-117.
15. Feller SM (2001). Crk family adaptors-signalling complex formation and biological roles. Oncogene 20, 6348-6371.
16. Fox DT, Homem CC, Myster SH, Wang F, Bain EE, Peifer M (2005). Rho1 regulates Drosophila adherens junctions independently of p120ctn. Development 132, 4819-4831.
17. Fox DT, Peifer M (2007). Abelson kinase (Abl) and RhoGEF2 regulate actin organization during cell constriction in Drosophila. Development 134, 567-578.
18. Gates J, Mahaffey JP, Rogers SL, Emerson M, Rogers EM, Sottile SL, Van Vactor D, Gertler FB, Peifer M (2007). Enabled plays key roles in embryonic epithelial morphogenesis in Drosophila. Development 134, 2027-2039.
19. Gertler FB, Comer AR, Juang JL, Ahern SM, Clark MJ, Liebl EC, Hoffmann FM (1995). enabled, a dosage-sensitive suppressor of mutations in the Drosophila Abl tyrosine kinase, encodes an Abl substrate with SH3 domain-binding properties. Genes Dev 9, 521-533.
20. Gertler FB, Hill KK, Clark MJ, Hoffmann FM (1993). Dosage-sensitive modifiers of Drosophila abl tyrosine kinase function: prospero, a regulator of axonal outgrowth, and disabled, a novel tyrosine kinase substrate. Genes Dev 7, 441-453.
21. Grevengoed EE, Fox DT, Gates J, Peifer M (2003). Balancing different types of actin polymerization at distinct sites: roles for Abelson kinase and Enabled. J Cell Biol 163, 1267-1279.
22. Grevengoed EE, Loureiro JJ, Jesse TL, Peifer M (2001). Abelson kinase regulates epithelial morphogenesis in Drosophila. J Cell Biol 155, 1185-1198.
23. Hantschel O, Superti-Furga G (2004). Regulation of the c-Abl and Bcr-Abl tyrosine kinases. Nat Rev Mol Cell Biol 5, 33-44.
24. Hardin JD, Boast S, Mendelsohn M, de los Santos K, Goff SP (1996). Transgenes encoding both type I and type IV c-abl proteins rescue the lethality of c-abl mutant mice. Oncogene 12, 2669-2677.
25. Heisterkamp N, Voncken JW, Senadheera D, Gonzalez-Gomez I, Reichert A, Haataja L, Reinikainen A, Pattengale PK, Groffen J (2000). Reduced oncogenicity of p190 Bcr/Abl F-actin-binding domain mutants. Blood 96, 2226-2232.
26. Henkemeyer M, West S, Gertler F, Hoffmann F (1990). A novel tyrosine kinase-independent function of Drosophila abl correlates with proper subcellular localization. Cell 63, 949-960.
27. Hernandez SE, Settleman J, Koleske AJ (2004). Adhesion-dependent regulation of p190RhoGAP in the developing brain by the Abl-related gene tyrosine kinase. Curr Biol 14, 691-696.
28. Hossain S, Dubielecka PM, Sikorski AF, Birge RB, Kotula L (2012). Crk and ABI1: binary molecular switches that regulate abl tyrosine kinase and signaling to the cytoskeleton. Genes Cancer 3, 402-413.
29. Huang YP, Comiskey EO, Dupree RS, Li SX, Koleske AJ, Burkhardt JK (2008). The c-Abl tyrosine kinase regulates actin remodeling at the immune synapse. Blood 112, 111-119.
30. Huettner CS, Zhang P, Van Etten RA, Tenen DG (2000). Reversibility of acute B-cell leukaemia induced by BCR-ABL1. Nat Genet 24, 57-60.
31. Hutson MS, Tokutake Y, Chang MS, Bloor JW, Venakides S, Kiehart DP, Edwards GS (2003). Forces for morphogenesis investigated with laser microsurgery and quantitative modeling. Science 300, 145-149.
32. Ibarra N, Pollitt A, Insall RH (2005). Regulation of actin assembly by SCAR/ WAVE proteins. Biochem Soc Trans 33, 1243-1246.
33. Ishimaru S, Ueda R, Hinohara Y, Ohtani M, Hanafusa H (2004). PVR plays a critical role via JNK activation in thorax closure during Drosophila metamorphosis. EMBO J 23, 3984-3994.
34. Kannan R, Kuzina I, Wincovitch S, Nowotarski SH, Giniger E (2014). The Abl/ enabled signaling pathway regulates Golgi architecture in Drosophila photoreceptor neurons. Mol Biol Cell 25, 2993-3005.
35. Khatri A, Wang J, Pendergast AM (2016). Multifunctional Abl kinases in health and disease. J Cell Sci 129, 9-16.
36. 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, 471-490.
37. Klinghoffer RA, Hamilton TG, Hoch R, Soriano P (2002). An allelic series at the PDGFalphaR locus indicates unequal contributions of distinct signaling pathways during development. Dev Cell 2, 103-113.
38. Koleske AJ, Gifford AM, Scott ML, Nee M, Bronson RT, Miczek KA, Baltimore D (1998). Essential roles for the Abl and Arg tyrosine kinases in neurulation. Neuron 21, 1259-1272.
39. Kunda P, Craig G, Dominguez V, Baum B (2003). Abi, Sra1, and Kette control the stability and localization of SCAR/WAVE to regulate the formation of actin-based protrusions. Curr Biol 13, 1867-1875.
40. Lapetina S, Mader CC, Machida K, Mayer BJ, Koleske AJ (2009). Arg interacts with cortactin to promote adhesion-dependent cell edge protrusion. J Cell Biol 185, 503-519.
41. Lee H, Engel U, Rusch J, Scherrer S, Sheard K, Van Vactor D (2004). The microtubule plus end tracking protein Orbit/MAST/CLASP acts downstream of the tyrosine kinase Abl in mediating axon guidance. Neuron 42, 913-926.
42. Li W, Li Y, Gao FB (2005). Abelson, enabled, and p120 catenin exert distinct effects on dendritic morphogenesis in Drosophila. Dev Dyn 234, 512-522.
43. Lin TY, Huang CH, Kao HH, Liou GG, Yeh SR, Cheng CM, Chen MH, Pan RL, Juang JL (2009). Abi plays an opposing role to Abl in Drosophila axonogenesis and synaptogenesis. Development 136, 3099-3107.
44. Lin YC, Yeckel MF, Koleske AJ (2013). Abl2/Arg controls dendritic spine and dendrite arbor stability via distinct cytoskeletal control pathways. J Neurosci 33, 1846-1857.
45. Mader CC, Oser M, Magalhaes MA, Bravo-Cordero JJ, Condeelis J, Koleske AJ, Gil-Henn H (2011). An EGFR-Src-Arg-cortactin pathway mediates functional maturation of invadopodia and breast cancer cell invasion. Cancer Res 71, 1730-1741.
46. Margolis B, Skolnik EY (1994). Activation of Ras by receptor tyrosine kinases. J Am Soc Nephrol 5, 1288-1299.
47. Martin P, Parkhurst SM (2004). Parallels between tissue repair and embryo morphogenesis. Development 131, 3021-3034.
48. McWhirter JR, Wang JY (1993). An actin-binding function contributes to transformation by the Bcr-Abl oncoprotein of Philadelphia chromosome-positive human leukemias. EMBO J 12, 1533-1546.
49. Miller AL, Wang Y, Mooseker MS, Koleske AJ (2004). The Abl-related gene (Arg) requires its F-actin-microtubule cross-linking activity to regulate lamellipodial dynamics during fibroblast adhesion. J Cell Biol 165, 407-419.
50. Miller MM, Lapetina S, MacGrath SM, Sfakianos MK, Pollard TD, Koleske AJ (2010). Regulation of actin polymerization and adhesion-dependent cell edge protrusion by the Abl-related gene (Arg) tyrosine kinase and N-WASp. Biochemistry 49, 2227-2234.
51. Mitra A, Radha V (2010). F-actin-binding domain of c-Abl regulates localized phosphorylation of C3G: role of C3G in c-Abl-mediated cell death. Oncogene 29, 4528-4542.
52. Moresco EM, Donaldson S, Williamson A, Koleske AJ (2005). Integrin-mediated dendrite branch maintenance requires Abelson (Abl) family kinases. J Neurosci 25, 6105-6118.
53. Moresco EM, Koleske AJ (2003). Regulation of neuronal morphogenesis and synaptic function by Abl family kinases. Curr Opin Neurobiol 13, 535-544.
54. O'Donnell MP, Bashaw GJ (2013). Distinct functional domains of the Abelson tyrosine kinase control axon guidance responses to Netrin and Slit to regulate the assembly of neural circuits. Development 140, 2724-2733.
55. O'Hare T, Corbin AS, Druker BJ (2005). Targeted CML therapy: controlling drug resistance, seeking cure. Curr Opin Genet Dev 16, 92-99.
56. Peacock JG, Miller AL, Bradley WD, Rodriguez OC, Webb DJ, Koleske AJ (2007). The abl-related gene tyrosine kinase acts through p190RhoGAP to inhibit actomyosin contractility and regulate focal adhesion dynamics upon adhesion to fibronectin. Mol Biol Cell 18, 3860-3872.
57. Pene-Dumitrescu T, Smithgall TE (2010). Expression of a Src family kinase in chronic myelogenous leukemia cells induces resistance to imatinib in a kinase-dependent manner. J Biol Chem 285, 21446-21457.
58. Pielage JF, Powell KR, Kalman D, Engel JN (2008). RNAi screen reveals an AbI kinase-dependent host cell pathway involved in Pseudomonas aeruginosa internalization. PLoS Pathog 4, e1000031.
59. Qiu Z, Cang Y, Goff SP (2010). c-Abl tyrosine kinase regulates cardiac growth and development. Proc Natl Acad Sci USA 107, 1136-1141.
60. Rock JM, Lim D, Stach L, Ogrodowicz RW, Keck JM, Jones MH, Wong CC, Yates JR, 3rd, Winey M, Smerdon SJ, et al. (2013). Activation of the yeast Hippo pathway by phosphorylation-dependent assembly of signaling complexes. Science 340, 871-875.
61. Ryu JR, Echarri A, Li R, Pendergast AM (2009). Regulation of cell-cell adhesion by Abi/Diaphanous complexes. Mol Cell Biol 29, 1735-1748.
62. Schindler T, Bornmann W, Pellicena P, Miller WT, Clarkson B, Kuriyan J (2000). Structural mechanism for STI-571 inhibition of abelson tyrosine kinase. Science 289, 1938-1942.
63. Schwartzberg PL, Stall AM, Hardin JD, Bowdish KS, Humaran T, Boast S, Harbison ML, Robertson EJ, Goff SP (1991). Mice homozygous for the ablm1 mutation show poor viability and depletion of selected B and T cell populations. Cell 65, 1165-1175.
64. Smith KM, Yacobi R, Van Etten RA (2003). Autoinhibition of Bcr-Abl through its SH3 domain. Mol Cell 12, 27-37.
65. Smith-Pearson PS, Greuber EK, Yogalingam G, Pendergast AM (2010). Abl kinases are required for invadopodia formation and chemokine-induced invasion. J Biol Chem 285, 40201-40211.
66. Stephan R, Gohl C, Fleige A, Klambt C, Bogdan S (2011). Membrane-targeted WAVE mediates photoreceptor axon targeting in the absence of the WAVE complex in Drosophila. Mol Biol Cell 22, 4079-4092.
67. Stevens TL, Rogers EM, Koontz LM, Fox DT, Homem CC, Nowotarski SH, Artabazon NB, Peifer M (2007). Using Bcr-Abl to examine mechanismsby which Abl kinase regulates morphogenesis in Drosophila. Mol Biol Cell 19, 378-393.
68. Stine RR, Greenspan LJ, Ramachandran KV, Matunis EL (2014). Coordinate regulation of stem cell competition by Slit-Robo and JAK-STAT signaling in the Drosophila testis. PLoS Genet 10, e1004713.
69. Tallquist MD, French WJ, Soriano P (2003). Additive effects of PDGF receptor beta signaling pathways in vascular smooth muscle cell development. PLoS Biol 1, E52.
70. Tamada M, Farrell DL, Zallen JA (2012). Abl regulates planar polarized junctional dynamics through beta-catenin tyrosine phosphorylation. Dev Cell 22, 309-319.
71. Underhill-Day N, Pierce A, Thompson SE, Xenaki D, Whetton AD, Owen-Lynch PJ (2006). Role of the C-terminal actin binding domain in BCR/ABL-mediated survival and drug resistance. Br J Haematol 132, 774-783.
72. van Etten RA, Jackson PK, Baltimore D, Sanders MC, Matsudeira PT, Janmey P (1994). The COOH terminus of the c-Abl tyrosine kinase contains distinct F- and G-actin binding domains with bundling activity. J Cell Biol 124, 325-340.
73. Wertheim JA, Perera SA, Hammer DA, Ren R, Boettiger D, Pear WS (2003). Localization of BCR-ABL to F-actin regulates cell adhesion but does not attenuate CML development. Blood 102, 2220-2228.
74. Wieschaus E, Nüsslein-Volhard C (1986). Looking at embryos. In: Drosophila, a Practical Approach, ed. DB Roberts, Oxford, UK: IRL Press, 199-228.
75. Woodring PJ, Hunter T, Wang JY (2001). Inhibition of c-Abl tyrosine kinase activity by filamentous actin. J Biol Chem 276, 27104-27110.
76. Zandy NL, Pendergast AM (2008). Abl tyrosine kinases modulate cadherin-dependent adhesion upstream and downstream of Rho family GTPases. Cell Cycle 7, 444-448.
77. Zhang XW, Ren RB (1998). Bcr-Abl efficiently induces a myeloproliferative disease and production of excess interleukin-3 and granulocyte-macrophage colony-stimulating factor in mice: A novel model for chronic myelogenous leukemia. Blood 92, 3829-3840.
78. Zulueta-Coarasa T, Tamada M, Lee EJ, Fernandez-Gonzalez R (2014). Automated multidimensional image analysis reveals a role for Abl in embryonic wound repair. Development 141, 2901-2911.