Drosophila melanogaster Acetyl-CoA-Carboxylase Sustains a Fatty Acid-Dependent Remote Signal to Waterproof the Respiratory System

PLoS Genetics

Volumn 8, Issue 8, 2012, Pages

  Parvy, Jean Philippe ^a,b   Napal, Laura ^a,c,f   Rubin, Thomas ^a,c,g   Poidevin, Mickael ^a,c   Perrin, Laurent ^d   Wicker Thomas, Claude ^e   Montagne, Jacques ^a,c  

^a CENTRE DE GÉNÉTIQUE MOLÉCULAIRE   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d AIX MARSEILLE UNIVERSITÉ   (France)

^e CNRS   (France)

^f INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^g INSTITUT CURIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; GLUCOSE; GLYCOGEN; TREHALOSE; TRIACYLGLYCEROL; VERY LONG CHAIN FATTY ACID;

ACETYL COENZYME A CARBOXYLASE GENE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EMBRYO; ENZYME ACTIVITY; FAT BODY; FATTY ACID METABOLISM; FATTY ACID SYNTHESIS; GENE; GENE DISRUPTION; GENE EXPRESSION; GENE INACTIVATION; GLYCOGEN SYNTHESIS; IMMUNODETECTION; INSECT CELL; LIPID TRANSPORT; LIVER FUNCTION; LUNG FUNCTION; NONHUMAN; OENOCYTE; PHENOTYPE; RESPIRATORY FUNCTION; RESPIRATORY SYSTEM; RNA INTERFERENCE; SPIRACLE ACTIVITY; SPIRACLE WATER TIGHTNESS;

ACETYL-COA CARBOXYLASE; ANIMALS; ANOXIA; CARBOHYDRATE METABOLISM; DROSOPHILA MELANOGASTER; FAT BODY; FATTY ACIDS; GLYCOGEN; LIPID METABOLISM; RESPIRATORY SYSTEM; RNA INTERFERENCE; TRIGLYCERIDES; WATER;

ANIMALIA; DROSOPHILA MELANOGASTER;

EID: 84866166159     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002925     Document Type: Article

References (72)

1. Lehrke M, Pascual G, Glass CK, Lazar MA, (2005) Gaining weight: the Keystone Symposium on PPAR and LXR. Genes Dev 19: 1737-1742.
2. Iwanaga T, Tsutsumi R, Noritake J, Fukata Y, Fukata M, (2009) Dynamic protein palmitoylation in cellular signaling. Prog Lipid Res 48: 117-127.
3. Brookheart RT, Michel CI, Schaffer JE, (2009) As a matter of fat. Cell Metab 10: 9-12.
4. Menendez JA, Lupu R, (2007) Fatty acid synthase and the lipogenic phenotype in cancer pathogenesis. Nat Rev Cancer 7: 763-777.
5. Menendez JA, Vazquez-Martin A, Ortega FJ, Fernandez-Real JM, (2009) Fatty acid synthase: association with insulin resistance, type 2 diabetes, and cancer. Clin Chem 55: 425-438.
6. Denechaud PD, Girard J, Postic C, (2008) Carbohydrate responsive element binding protein and lipid homeostasis. Curr Opin Lipidol 19: 301-306.
7. Lafontan M, Langin D, (2009) Lipolysis and lipid mobilization in human adipose tissue. Prog Lipid Res 48: 275-297.
8. Zechner R, Kienesberger PC, Haemmerle G, Zimmermann R, Lass A, (2009) Adipose triglyceride lipase and the lipolytic catabolism of cellular fat stores. J Lipid Res 50: 3-21.
9. Nagle CA, Klett EL, Coleman RA, (2009) Hepatic triacylglycerol accumulation and insulin resistance. J Lipid Res 50 Suppl: S74-79.
10. Baker KD, Thummel CS, (2007) Diabetic larvae and obese flies-emerging studies of metabolism in Drosophila. Cell Metab 6: 257-266.
11. Sieber MH, Thummel CS, (2009) The DHR96 nuclear receptor controls triacylglycerol homeostasis in Drosophila. Cell Metab 10: 481-490.
12. Wigglesworth VB, (1949) The utilization of reserve substances in Drosophila during flight. J Exp Biol 26: 150-163 illust.
13. Ruaud AF, Lam G, Thummel CS, (2011) The Drosophila NR4A nuclear receptor DHR38 regulates carbohydrate metabolism and glycogen storage. Mol Endocrinol 25: 83-91.
14. Gutierrez E, Wiggins D, Fielding B, Gould AP, (2007) Specialized hepatocyte-like cells regulate Drosophila lipid metabolism. Nature 445: 275-280.
15. Wheeler WM, (1892) Concerning the "blood-tissue" of the insecta. PSYCHE A Journal of Entomology 6: 216-220, 233-236, 254-258.
16. Manning G, Krasnow MA (1993) Development of the Drosophila tracheal system.; In Bate MaM-A, A (eds), editor. Cold Spring Harbor, NY.: Cold Spring Harbor Laboratory Press.
17. Barber MC, Price NT, Travers MT, (2005) Structure and regulation of acetyl-CoA carboxylase genes of metazoa. Biochim Biophys Acta 1733: 1-28.
18. Smith S, Tsai SC, (2007) The type I fatty acid and polyketide synthases: a tale of two megasynthases. Nat Prod Rep 24: 1041-1072.
19. Jakobsson A, Westerberg R, Jacobsson A, (2006) Fatty acid elongases in mammals: their regulation and roles in metabolism. Prog Lipid Res 45: 237-249.
20. Guillou H, Zadravec D, Martin PG, Jacobsson A, (2010) The key roles of elongases and desaturases in mammalian fatty acid metabolism: Insights from transgenic mice. Prog Lipid Res 49: 186-199.
21. Abu-Elheiga L, Matzuk MM, Kordari P, Oh W, Shaikenov T, et al. (2005) Mutant mice lacking acetyl-CoA carboxylase 1 are embryonically lethal. Proc Natl Acad Sci U S A 102: 12011-12016.
22. Abu-Elheiga L, Matzuk MM, Abo-Hashema KA, Wakil SJ, (2001) Continuous fatty acid oxidation and reduced fat storage in mice lacking acetyl-CoA carboxylase 2. Science 291: 2613-2616.
23. Morillas M, Gomez-Puertas P, Roca R, Serra D, Asins G, et al. (2001) Structural model of the catalytic core of carnitine palmitoyltransferase I and carnitine octanoyltransferase (COT): mutation of CPT I histidine 473 and alanine 381 and COT alanine 238 impairs the catalytic activity. J Biol Chem 276: 45001-45008.
24. Mao J, DeMayo FJ, Li H, Abu-Elheiga L, Gu Z, et al. (2006) Liver-specific deletion of acetyl-CoA carboxylase 1 reduces hepatic triglyceride accumulation without affecting glucose homeostasis. Proc Natl Acad Sci U S A 103: 8552-8557.
25. Mao J, Yang T, Gu Z, Heird WC, Finegold MJ, et al. (2009) aP2-Cre-mediated inactivation of acetyl-CoA carboxylase 1 causes growth retardation and reduced lipid accumulation in adipose tissues. Proc Natl Acad Sci U S A 106: 17576-17581.
26. Chirala SS, Chang H, Matzuk M, Abu-Elheiga L, Mao J, et al. (2003) Fatty acid synthesis is essential in embryonic development: fatty acid synthase null mutants and most of the heterozygotes die in utero. Proc Natl Acad Sci U S A 100: 6358-6363.
27. Chakravarthy MV, Pan Z, Zhu Y, Tordjman K, Schneider JG, et al. (2005) "New" hepatic fat activates PPARalpha to maintain glucose, lipid, and cholesterol homeostasis. Cell Metab 1: 309-322.
28. Dietzl G, Chen D, Schnorrer F, Su KC, Barinova Y, et al. (2007) A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448: 151-156.
29. Flybase (2003) The FlyBase database of the Drosophila genome projects and community literature. Nucleic Acids Res 31: 172-175.
30. Chintapalli VR, Wang J, Dow JA, (2007) Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat Genet 39: 715-720.
31. Parra-Peralbo E, Culi J, (2011) Drosophila lipophorin receptors mediate the uptake of neutral lipids in oocytes and imaginal disc cells by an endocytosis-independent mechanism. PLoS Genet 7: e1001297 doi:10.1371/journal.pgen.1001297.
32. Wingrove JA, O'Farrell PH, (1999) Nitric oxide contributes to behavioral, cellular, and developmental responses to low oxygen in Drosophila. Cell 98: 105-114.
33. Billeter JC, Atallah J, Krupp JJ, Millar JG, Levine JD, (2009) Specialized cells tag sexual and species identity in Drosophila melanogaster. Nature 461: 987-991.
34. Reiling JH, Hafen E, (2004) The hypoxia-induced paralogs Scylla and Charybdis inhibit growth by down-regulating S6K activity upstream of TSC in Drosophila. Genes Dev 18: 2879-2892.
35. Rizki MTM, (1956) The cytophysiology of the spiracular glands of Drosophila melanogaster. J Morphol 98: 497-511.
36. Jarial MS, Engstrom E, (1995) Fine structure of the spiracular glands in larval Drosophila melanogaster (MEIG.) (Diptera: Drosophilidae). Int J Insect Morphol & Embryol 24: 1-12.
37. Dantuma NP, Potters M, De Winther MP, Tensen CP, Kooiman FP, et al. (1999) An insect homolog of the vertebrate very low density lipoprotein receptor mediates endocytosis of lipophorins. J Lipid Res 40: 973-978.
38. Qatanani M, Lazar MA, (2007) Mechanisms of obesity-associated insulin resistance: many choices on the menu. Genes Dev 21: 1443-1455.
39. Agius L, (2008) Glucokinase and molecular aspects of liver glycogen metabolism. Biochem J 414: 1-18.
40. Krssak M, Brehm A, Bernroider E, Anderwald C, Nowotny P, et al. (2004) Alterations in postprandial hepatic glycogen metabolism in type 2 diabetes. Diabetes 53: 3048-3056.
41. Kir S, Beddow SA, Samuel VT, Miller P, Previs SF, et al. (2011) FGF19 as a postprandial, insulin-independent activator of hepatic protein and glycogen synthesis. Science 331: 1621-1624.
42. Docsa T, Czifrak K, Huse C, Somsak L, Gergely P, (2011) Effect of glucopyranosylidene-spiro-thiohydantoin on glycogen metabolism in liver tissues of streptozotocin-induced and obese diabetic rats. Mol Med Report 4: 477-481.
43. Cross DA, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA, (1995) Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378: 785-789.
44. 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: 1091-1101.
45. Gryzik T, Muller HA, (2004) FGF8-like1 and FGF8-like2 encode putative ligands of the FGF receptor Htl and are required for mesoderm migration in the Drosophila gastrula. Curr Biol 14: 659-667.
46. Albro HT, (1930) A cytological study of the changes occurring in the oenocytes of Galerucella nymphaeae Linn. during the larval and pupal periods of development. Journal of Morphology 50: 527-567.
47. Pospisilik JA, Schramek D, Schnidar H, Cronin SJ, Nehme NT, et al. (2010) Drosophila genome-wide obesity screen reveals hedgehog as a determinant of brown versus white adipose cell fate. Cell 140: 148-160.
48. Kraegen EW, Cooney GJ, Turner N, (2008) Muscle insulin resistance: a case of fat overconsumption, not mitochondrial dysfunction. Proc Natl Acad Sci U S A 105: 7627-7628.
49. Browning JD, Baxter J, Satapati S, Burgess SC, (2012) The effect of short-term fasting on liver and skeletal muscle lipid, glucose, and energy metabolism in healthy women and men. J Lipid Res 53: 577-586.
50. Martins GF, Ramalho-Ortigao JM, Lobo NF, Severson DW, McDowell MA, et al. (2011) Insights into the transcriptome of oenocytes from Aedes aegypti pupae. Mem Inst Oswaldo Cruz 106: 308-315.
51. Krupp JJ, Kent C, Billeter JC, Azanchi R, So AK, et al. (2008) Social experience modifies pheromone expression and mating behavior in male Drosophila melanogaster. Curr Biol 18: 1373-1383.
52. Kohler K, Brunner E, Guan XL, Boucke K, Greber UF, et al. (2009) A combined proteomic and genetic analysis identifies a role for the lipid desaturase Desat1 in starvation-induced autophagy in Drosophila. Autophagy 5: 980-990.
53. Wigglesworth VB, (1988) The source of lipids and polyphenols for the insect cuticle: The role of fat body, oenocytes and oenocytoids. Tissue Cell 20: 919-932.
54. Li Y, Paik YK, (2011) A potential role for fatty acid biosynthesis genes during molting and cuticle formation in Caenorhabditis elegans. BMB Rep 44: 285-290.
55. Hoffmann AA, Harshman LG, (1999) Desiccation and starvation resistance in Drosophila: patterns of variation at the species, population and intrapopulation levels. Heredity (Edinb) 83 (Pt 6):: 637-643.
56. Neven L, Mitcham E (2008) Controlled atmosphere technologies for insect control. In: Capinera JL, editor. Encyclopedia of entomology. New York: Springer. pp. 1046-1051.
57. Liu L, Johnson WA, Welsh MJ, (2003) Drosophila DEG/ENaC pickpocket genes are expressed in the tracheal system, where they may be involved in liquid clearance. Proc Natl Acad Sci U S A 100: 2128-2133.
58. Behr M, Wingen C, Wolf C, Schuh R, Hoch M, (2007) Wurst is essential for airway clearance and respiratory-tube size control. Nat Cell Biol 9: 847-853.
59. Zhang L, Ward REt, (2009) uninflatable encodes a novel ectodermal apical surface protein required for tracheal inflation in Drosophila. Dev Biol 336: 201-212.
60. Alvarez de la Rosa D, Canessa CM, Fyfe GK, Zhang P, (2000) Structure and regulation of amiloride-sensitive sodium channels. Annu Rev Physiol 62: 573-594.
61. Hummler E, Barker P, Gatzy J, Beermann F, Verdumo C, et al. (1996) Early death due to defective neonatal lung liquid clearance in alpha-ENaC-deficient mice. Nat Genet 12: 325-328.
62. Whitten J (1980) The tracheal system.: ed. M. Ashburner and T.R.F Wright. 499-540 p.
63. Asha H, Nagy I, Kovacs G, Stetson D, Ando I, et al. (2003) Analysis of Ras-induced overproliferation in Drosophila hemocytes. Genetics 163: 203-215.
64. Chen P, Nordstrom W, Gish B, Abrams JM, (1996) grim, a novel cell death gene in Drosophila. Genes Dev 10: 1773-1782.
65. Parks AL, Cook KR, Belvin M, Dompe NA, Fawcett R, et al. (2004) Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome. Nat Genet 36: 288-292.
66. Ye X, Liu Q, (2008) Expression, purification, and analysis of recombinant Drosophila Dicer-1 and Dicer-2 enzymes. Methods Mol Biol 442: 11-27.
67. Lee YS, Carthew RW, (2003) Making a better RNAi vector for Drosophila: use of intron spacers. Methods 30: 322-329.
68. Romeo Y, Lemaitre B, (2008) Drosophila immunity: methods for monitoring the activity of Toll and Imd signaling pathways. Methods Mol Biol 415: 379-394.
69. Miura S, Gan JW, Brzostowski J, Parisi MJ, Schultz CJ, et al. (2002) Functional conservation for lipid storage droplet association among Perilipin, ADRP, and TIP47 (PAT)-related proteins in mammals, Drosophila, and Dictyostelium. J Biol Chem 277: 32253-32257.
70. Meunier N, Belgacem YH, Martin JR, (2007) Regulation of feeding behaviour and locomotor activity by takeout in Drosophila. J Exp Biol 210: 1424-1434.
71. Dionne MS, Pham LN, Shirasu-Hiza M, Schneider DS, (2006) Akt and FOXO dysregulation contribute to infection-induced wasting in Drosophila. Curr Biol 16: 1977-1985.
72. Bathellier C, Tcherkez G, Mauve C, Bligny R, Gout E, et al. (2009) On the resilience of nitrogen assimilation by intact roots under starvation, as revealed by isotopic and metabolomic techniques. Rapid Commun Mass Spectrom 23: 2847-2856.