Mitotic Membrane Turnover Coordinates Differential Induction of the Heart Progenitor Lineage

Developmental Cell

Volumn 34, Issue 5, 2015, Pages 505-519

  Cota, Christina D ^a   Davidson, Brad ^a  

^a SWARTHMORE COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN; CD18 ANTIGEN; FIBROBLAST GROWTH FACTOR RECEPTOR; FIBROBLAST GROWTH FACTOR; INTEGRIN;

ANIMAL CELL; ARTICLE; CARDIAC STEM CELL; CELL ADHESION; CELL DIFFERENTIATION; CELL DIVISION; CELL LINEAGE; CELL POLARITY; CIONA INTESTINALIS; CONTROLLED STUDY; DAUGHTER CELL; EMBRYO; INTERNALIZATION; MITOSIS; MITOTIC MEMBRANE TURNOVER; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION; TURNOVER TIME; ANIMAL; ANIMAL EMBRYO; CYTOLOGY; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; HEART; HEART MUSCLE; METABOLISM; PHYSIOLOGY; PROCEDURES;

ANIMALS; CELL ADHESION; CELL DIVISION; CELL LINEAGE; CIONA INTESTINALIS; EMBRYO, NONMAMMALIAN; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEART; INTEGRINS; MYOCARDIUM; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 84942328514     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2015.07.001     Document Type: Article

References (81)

1. Anthis N.J., Haling J.R., Oxley C.L., Memo M., Wegener K.L., Lim C.J., Ginsberg M.H., Campbell I.D. β integrin tyrosine phosphorylation is a conserved mechanism for regulating talin-induced integrin activation. J. Biol. Chem. 2009, 284:36700-36710.
2. Beh J., Shi W., Levine M., Davidson B., Christiaen L. FoxF is essential for FGF-induced migration of heart progenitor cells in the ascidian Ciona intestinalis. Development 2007, 134:3297-3305.
3. Boettner B., Van Aelst L. Control of cell adhesion dynamics by Rap1 signaling. Curr. Opin. Cell Biol. 2009, 21:684-693.
4. Bonaventure J., Horne W.C., Baron R. The localization of FGFR3 mutations causing thanatophoric dysplasia type I differentially affects phosphorylation, processing and ubiquitylation of the receptor. FEBS J. 2007, 274:3078-3093.
5. Boucrot E., Kirchhausen T. Endosomal recycling controls plasma membrane area during mitosis. Proc. Natl. Acad. Sci. USA 2007, 104:7939-7944.
6. Boucrot E., Howes M.T., Kirchhausen T., Parton R.G. Redistribution of caveolae during mitosis. J. Cell Sci. 2011, 124:1965-1972.
7. Brunet T., Bouclet A., Ahmadi P., Mitrossilis D., Driquez B., Brunet A.-C., Henry L., Serman F., Béalle G., Ménager C., et al. Evolutionary conservation of early mesoderm specification by mechanotransduction in Bilateria. Nat. Commun. 2013, 4:2821.
8. Bryant M.R., Marta C.B., Kim F.S., Bansal R. Phosphorylation and lipid raft association of fibroblast growth factor receptor-2 in oligodendrocytes. Glia 2009, 57:935-946.
9. Calderwood D.A., Fujioka Y., de Pereda J.M., García-Alvarez B., Nakamoto T., Margolis B., McGlade C.J., Liddington R.C., Ginsberg M.H. Integrin beta cytoplasmic domain interactions with phosphotyrosine-binding domains: a structural prototype for diversity in integrin signaling. Proc. Natl. Acad. Sci. USA 2003, 100:2272-2277.
10. Caswell P., Norman J. Endocytic transport of integrins during cell migration and invasion. Trends Cell Biol. 2008, 18:257-263.
11. Caswell P.T., Vadrevu S., Norman J.C. Integrins: masters and slaves of endocytic transport. Nat. Rev. Mol. Cell Biol. 2009, 10:843-853.
12. Cerezo A., Guadamillas M.C., Goetz J.G., Sánchez-Perales S., Klein E., Assoian R.K., del Pozo M.A. The absence of caveolin-1 increases proliferation and anchorage- independent growth by a Rac-dependent, Erk-independent mechanism. Mol. Cell. Biol. 2009, 29:5046-5059.
13. Cooley J., Whitaker S., Sweeney S., Fraser S., Davidson B. Cytoskeletal polarity mediates localized induction of the heart progenitor lineage. Nat. Cell Biol. 2011, 13:952-957.
14. Corbo J.C., Levine M., Zeller R.W. Characterization of a notochord-specific enhancer from the Brachyury promoter region of the ascidian, Ciona intestinalis. Development 1997, 124:589-602.
15. Cota C.D., Segade F., Davidson B. Heart genetics in a small package, exploiting the condensed genome of Ciona intestinalis. Brief. Funct. Genomics 2014, 13:3-14.
16. Dave P.C., Dingal P., Discher D.E. Material control of stem cell differentiation: challenges in nano-characterization. Curr. Opin. Biotechnol. 2014, 28:46-50.
17. Davidson B. Ciona intestinalis as a model for cardiac development. Semin. Cell Dev. Biol. 2007, 18:16-26.
18. Davidson B., Levine M. Evolutionary origins of the vertebrate heart: Specification of the cardiac lineage in Ciona intestinalis. Proc. Natl. Acad. Sci. USA 2003, 100:11469-11473.
19. Davidson B., Shi W., Levine M. Uncoupling heart cell specification and migration in the simple chordate Ciona intestinalis. Development 2005, 132:4811-4818.
20. Davidson B., Shi W., Beh J., Christiaen L., Levine M. FGF signaling delineates the cardiac progenitor field in the simple chordate, Ciona intestinalis. Genes Dev. 2006, 20:2728-2738.
21. Dehal P., Satou Y., Campbell R.K., Chapman J., Degnan B., De Tomaso A., Davidson B., Di Gregorio A., Gelpke M., Goodstein D.M., et al. The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 2002, 298:2157-2167.
22. del Pozo M.A., Alderson N.B., Kiosses W.B., Chiang H.-H., Anderson R.G.W., Schwartz M.A. Integrins regulate Rac targeting by internalization of membrane domains. Science 2004, 303:839-842.
23. del Pozo M.A., Balasubramanian N., Alderson N.B., Kiosses W.B., Grande-García A., Anderson R.G.W., Schwartz M.A. Phospho-caveolin-1 mediates integrin-regulated membrane domain internalization. Nat. Cell Biol. 2005, 7:901-908.
24. Delcommenne M., Tan C., Gray V., Rue L., Woodgett J., Dedhar S. Phosphoinositide-3-OH kinase-dependent regulation of glycogen synthase kinase 3 and protein kinase B/AKT by the integrin-linked kinase. Proc. Natl. Acad. Sci. USA 1998, 95:11211-11216.
25. Di Guglielmo G.M., Le Roy C., Goodfellow A.F., Wrana J.L. Distinct endocytic pathways regulate TGF-beta receptor signalling and turnover. Nat. Cell Biol. 2003, 5:410-421.
26. Du J., Chen X., Liang X., Zhang G., Xu J., He L., Zhan Q., Feng X.-Q., Chien S., Yang C. Integrin activation and internalization on soft ECM as a mechanism of induction of stem cell differentiation by ECM elasticity. Proc. Natl. Acad. Sci. USA 2011, 108:9466-9471.
27. Engler A.J., Sen S., Sweeney H.L., Discher D.E. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126:677-689.
28. Farge E. Mechanotransduction in development. Curr. Top. Dev. Biol. 2011, 95:243-265.
29. Fonar Y., Gutkovich Y.E., Root H., Malyarova A., Aamar E., Golubovskaya V.M., Elias S., Elkouby Y.M., Frank D. Focal adhesion kinase protein regulates Wnt3a gene expression to control cell fate specification in the developing neural plate. Mol. Biol. Cell 2011, 22:2409-2421.
30. Fürthauer M., González-Gaitán M. Endocytosis and mitosis: a two-way relationship. Cell Cycle 2009, 8:3311-3318.
31. Goh L.K., Sorkin A. Endocytosis of receptor tyrosine kinases. Cold Spring Harb. Perspect. Biol. 2013, 5:a017459.
32. Goulas S., Conder R., Knoblich J.A. The Par complex and integrins direct asymmetric cell division in adult intestinal stem cells. Cell Stem Cell 2012, 11:529-540.
33. Guadamillas M.C., Cerezo A., Del Pozo M.A. Overcoming anoikis--pathways to anchorage-independent growth in cancer. J. Cell Sci. 2011, 124:3189-3197.
34. Harvey R.D., Calaghan S.C. Caveolae create local signalling domains through their distinct protein content, lipid profile and morphology. J. Mol. Cell. Cardiol. 2012, 52:366-375.
35. Hatch N.E., Hudson M., Seto M.L., Cunningham M.L., Bothwell M. Intracellular retention, degradation, and signaling of glycosylation-deficient FGFR2 and craniosynostosis syndrome-associated FGFR2C278F. J. Biol. Chem. 2006, 281:27292-27305.
36. Hotta K., Mitsuhara K., Takahashi H., Inaba K., Oka K., Gojobori T., Ikeo K. A web-based interactive developmental table for the ascidian Ciona intestinalis, including 3D real-image embryo reconstructions: I. From fertilized egg to hatching larva. Dev. Dyn. 2007, 236:1790-1805.
37. Hu P., Luo B.H. Integrin bi-directional signaling across the plasma membrane. J. Cell. Physiol. 2013, 228:306-312.
38. Huttenlocher A., Horwitz A.R. Integrins in cell migration. Cold Spring Harb. Perspect. Biol. 2011, 3:a005074.
39. Ivaska J., Heino J. Cooperation between integrins and growth factor receptors in signaling and endocytosis. Annu. Rev. Cell Dev. Biol. 2011, 27:291-320.
40. Kaabeche K., Lemonnier J., Le Mée S., Caverzasio J., Marie P.J. Cbl-mediated degradation of Lyn and Fyn induced by constitutive fibroblast growth factor receptor-2 activation supports osteoblast differentiation. J. Biol. Chem. 2004, 279:36259-36267.
41. Kim S.-H., Turnbull J., Guimond S. Extracellular matrix and cell signalling: the dynamic cooperation of integrin, proteoglycan and growth factor receptor. J. Endocrinol. 2011, 209:139-151.
42. LaFlamme S.E., Nieves B., Colello D., Reverte C.G. Integrins as regulators of the mitotic machinery. Curr. Opin. Cell Biol. 2008, 20:576-582.
43. Lee H., Park D.S., Razani B., Russell R.G., Pestell R.G., Lisanti M.P. Caveolin-1 mutations (P132L and null) and the pathogenesis of breast cancer: caveolin-1 (P132L) behaves in a dominant-negative manner and caveolin-1 (-/-) null mice show mammary epithelial cell hyperplasia. Am. J. Pathol. 2002, 161:1357-1369.
44. Legate K.R., Wickström S.A., Fässler R. Genetic and cell biological analysis of integrin outside-in signaling. Genes Dev. 2009, 23:397-418.
45. Lemaire P. Evolutionary crossroads in developmental biology: the tunicates. Development 2011, 138:2143-2152.
46. Liu S., Calderwood D.A., Ginsberg M.H. Integrin cytoplasmic domain-binding proteins. J. Cell Sci. 2000, 113:3563-3571.
47. Martin-Bermudo M.D. Integrins modulate the Egfr signaling pathway to regulate tendon cell differentiation in the Drosophila embryo. Development 2000, 127:2607-2615.
48. McKay H.F., Burgess D.R. 'Life is a highway': membrane trafficking during cytokinesis. Traffic 2011, 12:247-251.
49. Miller C.J., Davidson L.A. The interplay between cell signalling and mechanics in developmental processes. Nat. Rev. Genet. 2013, 14:733-744.
50. Monsonego-Ornan E., Adar R., Rom E., Yayon A. FGF receptors ubiquitylation: dependence on tyrosine kinase activity and role in downregulation. FEBS Lett. 2002, 528:83-89.
51. Montagnac G., Echard A., Chavrier P. Endocytic traffic in animal cell cytokinesis. Curr. Opin. Cell Biol. 2008, 20:454-461.
52. Moser M., Legate K.R., Zent R., Fässler R. The tail of integrins, talin, and kindlins. Science 2009, 324:895-899.
53. Nishimura T., Kaibuchi K. Numb controls integrin endocytosis for directional cell migration with aPKC and PAR-3. Dev. Cell 2007, 13:15-28.
54. Norton J., Cooley J., Islam A.F.M.T., Cota C.D., Davidson B. Matrix adhesion polarizes heart progenitor induction in the invertebrate chordate Ciona intestinalis. Development 2013, 140:1301-1311.
55. Nowak M., Machate A., Yu S.R., Gupta M., Brand M. Interpretation of the FGF8 morphogen gradient is regulated by endocytic trafficking. Nat. Cell Biol. 2011, 13:153-158.
56. Parton R.G., del Pozo M.A. Caveolae as plasma membrane sensors, protectors and organizers. Nat. Rev. Mol. Cell Biol. 2013, 14:98-112.
57. Patel H.H., Murray F., Insel P.A. Caveolae as organizers of pharmacologically relevant signal transduction molecules. Annu. Rev. Pharmacol. Toxicol. 2008, 48:359-391.
58. Pellinen T., Tuomi S., Arjonen A., Wolf M., Edgren H., Meyer H., Grosse R., Kitzing T., Rantala J.K., Kallioniemi O., et al. Integrin trafficking regulated by Rab21 is necessary for cytokinesis. Dev. Cell 2008, 15:371-385.
59. Radel C., Rizzo V. Integrin mechanotransduction stimulates caveolin-1 phosphorylation and recruitment of Csk to mediate actin reorganization. Am. J. Physiol. Heart Circ. Physiol. 2005, 288:H936-H945.
60. Reilly G.C., Engler A.J. Intrinsic extracellular matrix properties regulate stem cell differentiation. J. Biomech. 2010, 43:55-62.
61. Salanueva I.J., Cerezo A., Guadamillas M.C., del Pozo M.A. Integrin regulation of caveolin function. J. Cell. Mol. Med. 2007, 11:969-980.
62. Sasaki H., Yoshida K., Hozumi A., Sasakura Y. CRISPR/Cas9-mediated gene knockout in the ascidian Ciona intestinalis. Dev. Growth Differ. 2014, 56:499-510.
63. Satou Y., Yamada L., Mochizuki Y., Takatori N., Kawashima T., Sasaki A., Hamaguchi M., Awazu S., Yagi K., Sasakura Y., et al. A cDNA resource from the basal chordate Ciona intestinalis. Genesis 2002, 33:153-154.
64. Schmidt-Glenewinkel H., Reinz E., Bulashevska S., Beaudouin J., Legewie S., Alonso A., Eils R. Multiparametric image analysis reveals role of Caveolin1 in endosomal progression rather than internalization of EGFR. FEBS Lett. 2012, 586:1179-1189.
65. Shatz M., Lustig G., Reich R., Liscovitch M. Caveolin-1 mutants P132L and Y14F are dominant negative regulators of invasion, migration and aggregation in H1299 lung cancer cells. Exp. Cell Res. 2010, 316:1748-1762.
66. Shibue T., Weinberg R.A. Integrin beta1-focal adhesion kinase signaling directs the proliferation of metastatic cancer cells disseminated in the lungs. Proc. Natl. Acad. Sci. USA 2009, 106:10290-10295.
67. Shrestha R., Little K.A., Tamayo J.V., Li W., Perlman D.H., Devenport D. Mitotic control of planar cell polarity by Polo-like Kinase 1. Dev. Cell 2015, 33:522-534.
68. Singh R.D., Holicky E.L., Cheng Z.-J., Kim S.-Y., Wheatley C.L., Marks D.L., Bittman R., Pagano R.E. Inhibition of caveolar uptake, SV40 infection, and beta1-integrin signaling by a nonnatural glycosphingolipid stereoisomer. J. Cell Biol. 2007, 176:895-901.
69. Stolfi A., Christiaen L. Genetic and genomic toolbox of the chordate Ciona intestinalis. Genetics 2012, 192:55-66.
70. Stolfi A., Gandhi S., Salek F., Christiaen L. Tissue-specific genome editing in Ciona embryos by CRISPR/Cas9. Development 2014, 141:4115-4120.
71. Strålfors P. Caveolins and caveolae, roles in insulin signalling and diabetes. Adv. Exp. Med. Biol. 2012, 729:111-126.
72. Streuli C.H. Integrins and cell-fate determination. J. Cell Sci. 2009, 122:171-177.
73. Streuli C.H., Akhtar N. Signal co-operation between integrins and other receptor systems. Biochem. J. 2009, 418:491-506.
74. Tacheva-Grigorova S.K., Santos A.J.M., Boucrot E., Kirchhausen T. Clathrin-mediated endocytosis persists during unperturbed mitosis. Cell Rep. 2013, 4:659-668.
75. Teckchandani A., Toida N., Goodchild J., Henderson C., Watts J., Wollscheid B., Cooper J.A. Quantitative proteomics identifies a Dab2/integrin module regulating cell migration. J. Cell Biol. 2009, 186:99-111.
76. Toyoshima F., Nishida E. Spindle orientation in animal cell mitosis: roles of integrin in the control of spindle axis. J. Cell. Physiol. 2007, 213:407-411.
77. Wickström S.A., Lange A., Hess M.W., Polleux J., Spatz J.P., Krüger M., Pfaller K., Lambacher A., Bloch W., Mann M., et al. Integrin-linked kinase controls microtubule dynamics required for plasma membrane targeting of caveolae. Dev. Cell 2010, 19:574-588.
78. Woznica A., Haeussler M., Starobinska E., Jemmett J., Li Y., Mount D., Davidson B. Initial deployment of the cardiogenic gene regulatory network in the basal chordate, Ciona intestinalis. Dev. Biol. 2012, 368:127-139.
79. Yamashita Y.M., Yuan H., Cheng J., Hunt A.J. Polarity in stem cell division: asymmetric stem cell division in tissue homeostasis. Cold Spring Harb. Perspect. Biol. 2010, 2. a001313-a001313.
80. Yim E.K.F., Sheetz M.P. Force-dependent cell signaling in stem cell differentiation. Stem Cell Res. Ther. 2012, 3:41.
81. Zhou Y., Liang H., Rodkey T., Ariotti N., Parton R.G., Hancock J.F. Signal integration by lipid-mediated spatial cross talk between Ras nanoclusters. Mol. Cell. Biol. 2014, 34:862-876.