Microsomal triacylglycerol transfer protein (MTP) is required to expand tracheal lumen in Drosophila in a cell-autonomous manner

Journal of Cell Science

Volumn 125, Issue 24, 2012, Pages 6038-6048

  Baer, Magdalena M ^a,b   Palm, Wilhelm ^c   Eaton, Suzanne ^c   Leptin, Maria ^b,d   Affolter, Markus ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b UNIVERSITY OF COLOGNE   (Germany)

^c MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^d EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

Lumen expansion; Trachea; Tubulogenesis; Unicellular tubes

Indexed keywords

MICROSOMAL TRIGLYCERIDE TRANSFER PROTEIN; CARRIER PROTEIN; TRIACYLGLYCEROL;

ALLELE; ANIMAL CELL; ANIMAL TISSUE; APICAL MEMBRANE; ARTICLE; CELL EXPANSION; CELL MATURATION; CONTROLLED STUDY; DROSOPHILA; GENE; GENE MUTATION; GENETIC CODE; LARVA; LIPOPROTEIN METABOLISM; LIPOPROTEIN SECRETION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; TRACHEA; ANIMAL; ANIMAL MODEL; FEMALE; GENETICS; MALE; METABOLISM;

ANIMALS; CARRIER PROTEINS; DROSOPHILA; FEMALE; MALE; MODELS, ANIMAL; TRACHEA; TRIGLYCERIDES;

EID: 84875591423     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.110452     Document Type: Article

References (47)

1. Affolter, M. and Caussinus, E. (2008). Tracheal branching morphogenesis in Drosophila: new insights into cell behaviour and organ architecture. Development 135, 2055-2064.
2. Affolter, M., Zeller, R. and Caussinus, E. (2009). Tissue remodelling through branching morphogenesis. Nat. Rev. Mol. Cell Biol. 10, 831-842.
3. Andrew, D. J. and Ewald, A. J. (2010). Morphogenesis of epithelial tubes: Insights into tube formation, elongation, and elaboration. Dev. Biol. 341, 34-55.
4. Armbruster, K. and Luschnig, S. (2012). The Drosophila Sec7 domain guanine nucleotide exchange factor protein Gartenzwerg localizes at the cis-Golgi and is essential for epithelial tube expansion. J. Cell Sci. 125, 1318-1328.
5. Atzel, A. and Wetterau, J. R. (1993). Mechanism of microsomal triglyceride transfer protein catalyzed lipid transport. Biochemistry 32, 10444-10450.
6. Atzel, A. and Wetterau, J. R. (1994). Identification of two classes of lipid molecule binding sites on the microsomal triglyceride transfer protein. Biochemistry 33, 15382- 15388.
7. Baer, M. M., Bilstein, A. and Leptin, M. (2007). A clonal genetic screen for mutants causing defects in larval tracheal morphogenesis in Drosophila. Genetics 176, 2279-2291.
8. Baer, M. M., Chanut-Delalande, H. and Affolter, M. (2009). Cellular and molecular mechanisms underlying the formation of biological tubes. Curr. Top. Dev. Biol. 89, 137-162.
9. Berger J., Suzuki, T., Senti, K. A., Stubbs, J., Schaffner, G. and Dickson, B. J. (2001). Genetic mapping with SNP markers in Drosophila. Nat. Genet. 29, 475-481.
10. Bischof, J., Maeda, R. K., Hediger, M., Karch, F. and Basler, K. (2007). An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl. Acad. Sci. USA 104, 3312-3317.
11. Brozovic, S., Nagaishi, T., Yoshida, M., Betz, S., Salas, A., Chen, D., Kaser, A., Glickman, J., Kuo, T., Little, A. et al. (2004). CD1d function is regulated by microsomal triglyceride transfer protein. Nat. Med. 10, 535-539.
12. Chen, J., Honeyager, S. M., Schleede, J., Avanesov, A., Laughon, A. and Blair, S. S. (2012). Crossveinless d is a vitellogenin-like lipoprotein that binds BMPs and HSPGs, and is required for normal BMP signaling in the Drosophila wing. Development 139, 2170-2176.
13. Chintapalli, V. R., Wang, J. and Dow, J. A. (2007). Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat. Genet. 39, 715-720.
14. Dougan, S. K., Salas, A., Rava, P., Agyemang, A., Kaser, A., Morrison, J., Khurana, A., Kronenberg, M., Johnson, C., Exley, M. et al. (2005). Microsomal triglyceride transfer protein lipidation and control of CD1d on antigen-presenting cells. J. Exp. Med. 202, 529-539.
15. Eugster, C., Panáková , D., Mahmoud, A. and Eaton, S. (2007). Lipoprotein-heparan sulfate interactions in the Hh pathway. Dev. Cell 13, 57-71.
16. Forster, D., Armbruster, K. and Luschnig, S. (2010). Sec24-dependent secretion drives cell-autonomous expansion of tracheal tubes in Drosophila. Curr. Biol. 20, 62-68.
17. Gervais, L. and Casanova, J. (2010). In vivo coupling of cell elongation and lumen formation in a single cell. Curr. Biol. 20, 359-366.
18. Ghabrial, A., Luschnig, S., Metzstein, M. M. and Krasnow, M. A. (2003). Branching morphogenesis of the Drosophila tracheal system. Annu. Rev. Cell Dev. Biol. 19, 623-647.
19. Ghabrial, A. S., Levi, B. P. and Krasnow, M. A. (2011). A systematic screen for tube morphogenesis and branching genes in the Drosophila tracheal system. PLoS Genet. 7, e1002087.
20. Gordon, D. A., Jamil, H., Gregg, R. E., Olofsson, S. O. and Borén, J. (1996). Inhibition of the microsomal triglyceride transfer protein blocks the first step of apolipoprotein B lipoprotein assembly but not the addition of bulk core lipids in the second step. J. Biol. Chem. 271, 33047-33053.
21. Grieder, N. C., Caussinus, E., Parker, D. S., Cadigan, K., Affolter, M. and Luschnig, S. (2008). gammaCOP is required for apical protein secretion and epithelial morphogenesis in Drosophila melanogaster. PLoS ONE 3, e3241.
22. Hussain, M. M., Shi, J. and Dreizen, P. (2003a). Microsomal triglyceride transfer protein and its role in apoB-lipoprotein assembly. J. Lipid Res. 44, 22-32.
23. Hussain, M. M., Iqbal, J., Anwar, K., Rava, P. and Dai, K. (2003b). Microsomal triglyceride transfer protein: a multifunctional protein. Front. Biosci. 8, s500-s506.
24. Jayaram, S. A., Senti, K. A., Tiklova, K., Tsarouhas, V., Hemphala, J. and Samakovlis, C. (2008). COPI vesicle transport is a common requirement for tube expansion in Drosophila. PLoS ONE 3, e1964.
25. Jaźwińska, A., Ribeiro, C. and Affolter, M. (2003). Epithelial tube morphogenesis during Drosophila tracheal development requires Piopio, a luminal ZP protein. Nat. Cell Biol. 5, 895-901.
26. Kaser, A., Hava, D. L., Dougan, S. K., Chen, Z., Zeissig, S., Brenner, M. B. and Blumberg, R. S. (2008). Microsomal triglyceride transfer protein regulates endogenous and exogenous antigen presentation by group 1 CD1 molecules. Eur. J. Immunol. 38, 2351-2359.
27. Khatun, I., Zeissig, S., Iqbal, J., Wang, M., Curiel, D., Shelness, G. S., Blumberg, R. S. and Hussain, M. M. (2012). The phospholipid transfer activity of MTP produces apoB-lipoproteins and reduces hepatosteatosis while maintaining low plasma lipids. Hepatology 55, 1356-1368.
28. Le, T., Liang, Z., Patel, H., Yu, M. H., Sivasubramaniam, G., Slovitt, M., Tanentzapf, G., Mohanty, N., Paul, S. M., Wu, V. M. et al. (2006). A new family of Drosophila balancer chromosomes with a w-dfd-GMR yellow fluorescent protein marker. Genetics 174, 2255-2257.
29. Lubarsky, B. and Krasnow, M. A. (2003). Tube morphogenesis: making and shaping biological tubes. Cell 112, 19-28.
30. Luschnig, S., Bätz, T., Armbruster, K. and Krasnow, M. A. (2006). serpentine and zvermiform encode matrix proteins with chitin binding and deacetylation domains that limit tracheal tube length in Drosophila. Curr. Biol. 16, 186-194.
31. Norum, M., Tång, E., Chavoshi, T., Schwarz, H., Linke, D., Uv, A. and Moussian, B. (2010). Trafficking through COPII stabilises cell polarity and drives secretion during Drosophila epidermal differentiation. PLoS ONE 5, e10802.
32. Olofsson, S. O., Asp, L. and Borén, J. (1999). The assembly and secretion of apolipoprotein B-containing lipoproteins. Curr. Opin. Lipidol. 10, 341-346.
33. Palm, W., Sampaio, J. L., Brankatschk, M., Carvalho, M., Mahmoud, A., Shevchenko, A. and Eaton, S. (2012). Lipoproteins in Drosophila melanogaster -assembly, function, and influence on tissue lipid composition. PLoS Genet. 8, e1002828.
34. Panáková, D., Sprong, H., Marois, E., Thiele, C. and Eaton, S. (2005). Lipoprotein particles are required for Hedgehog and Wingless signalling. Nature 435, 58-65.
35. Raabe, M., Véniant, M. M., Sullivan, M. A., Zlot, C. H., Björkegren, J., Nielsen, L. B., Wong, J. S., Hamilton, R. L. and Young, S. G. (1999). Analysis of the role of microsomal triglyceride transfer protein in the liver of tissue-specific knockout mice. J. Clin. Invest. 103, 1287-1298.
36. Rava, P.,Ojakian,G.K., Shelness, G. S. andHussain,M.M. (2006). Phospholipid transfer activity of microsomal triacylglycerol transfer protein is sufficient for the assembly and secretion of apolipoprotein B lipoproteins. J. Biol. Chem. 281, 11019-11027.
37. Ribeiro, C., Neumann, M. and Affolter, M. (2004). Genetic control of cell intercalation during tracheal morphogenesis in Drosophila. Curr. Biol. 14, 2197-2207.
38. Sagiv, Y., Bai, L., Wei, D. G., Agami, R., Savage, P. B., Teyton, L. and Bendelac, A. (2007). A distal effect of microsomal triglyceride transfer protein deficiency on the lysosomal recycling of CD1d. J. Exp. Med. 204, 921-928.
39. Schottenfeld, J., Song, Y. and Ghabrial, A. S. (2010). Tube continued: morphogenesis of the Drosophila tracheal system. Curr. Opin. Cell Biol. 22, 633-639.
40. Sellers, J. A., Hou, L., Athar, H., Hussain, M. M. and Shelness, G. S. (2003). A Drosophila microsomal triglyceride transfer protein homolog promotes the assembly and secretion of human apolipoprotein B. Implications for human and insect transport and metabolism. J. Biol. Chem. 278, 20367-20373.
41. Smolenaars, M. M., Madsen, O., Rodenburg, K. W. and Van der Horst, D. J. (2007). Molecular diversity and evolution of the large lipid transfer protein superfamily. J. Lipid Res. 48, 489-502.
42. Swanson, L. E. and Beitel, G. J. (2006). Tubulogenesis: an inside job. Curr. Biol. 16, R51-R53.
43. Tsarouhas, V., Senti, K. A., Jayaram, S. A., Tiklová, K., Hemphälä , J., Adler, J. and Samakovlis, C. (2007). Sequential pulses of apical epithelial secretion and endocytosis drive airway maturation in Drosophila. Dev. Cell 13, 214-225.
44. Uv, A., Cantera, R. and Samakovlis, C. (2003). Drosophila tracheal morphogenesis: intricate cellular solutions to basic plumbing problems. Trends Cell Biol. 13, 301-309.
45. Wang, S., Meyer, H., Ochoa-Espinosa, A., Buchwald, U., Onel, S., Altenhein, B., Heinisch, J. J., Affolter, M. and Paululat, A. (2012). GBF1 (Gartenzwerg)-dependent secretion is required for Drosophila tubulogenesis. J. Cell Sci. 125, 461-472.
46. Zeissig, S., Dougan, S. K., Barral, D. C., Junker, Y., Chen, Z., Kaser, A., Ho, M., Mandel, H., McIntyre, A., Kennedy, S. M. et al. (2010). Primary deficiency of microsomal triglyceride transfer protein in human abetalipoproteinemia is associated with loss of CD1 function. J. Clin. Invest. 120, 2889-2899.
47. Zhang, L. and Ward, R. E., 4th (2009). uninflatable encodes a novel ectodermal apical surface protein required for tracheal inflation in Drosophila. Dev. Biol. 336, 201-212.