Grasshopper Lazarillo, a GPI-anchored Lipocalin, increases Drosophila longevity and stress resistance, and functionally replaces its secreted homolog NLaz

Insect Biochemistry and Molecular Biology

Volumn 42, Issue 10, 2012, Pages 776-789

  Ruiz, Mario ^a   Wicker Thomas, Claude ^b   Sanchez, Diego ^a   Ganfornina, Maria D ^a  

^a UNIVERSITY OF VALLADOLID   (Spain)

^b CNRS   (France)

Author keywords

Aging; Lipid storage; Lipocalin; NLaz; Oxidative stress

Indexed keywords

GLYCOSYLPHOSPHATIDYLINOSITOL; INSECT PROTEIN; LIPOCALIN;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CAELIFERA; CHEMISTRY; DROSOPHILA; EVOLUTION; FEMALE; GENETICS; MALE; METABOLISM; MOLECULAR GENETICS; OXIDATIVE STRESS; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL EVOLUTION; DROSOPHILA; FEMALE; GLYCOSYLPHOSPHATIDYLINOSITOLS; GRASSHOPPERS; INSECT PROTEINS; LIPOCALINS; MALE; MOLECULAR SEQUENCE DATA; OXIDATIVE STRESS; SEQUENCE ALIGNMENT; STRESS, PHYSIOLOGICAL;

SCHISTOCERCA AMERICANA; VERTEBRATA;

EID: 84865861259     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2012.07.005     Document Type: Article

References (68)

1. Akerström B., Borregaard N., Flover D., Salier J. Lipocalins 2006, Texas, Georgetown.
2. Bajo-Graneras R., Ganfornina M.D., Martin-Tejedor E., Sanchez D. Apolipoprotein D mediates autocrine protection of astrocytes and controls their reactivity level, contributing to the functional maintenance of paraquat-challenged dopaminergic systems. Glia 2011, 59:1551-1566.
3. Bajo-Graneras R., Sanchez D., Gutierrez G., Gonzalez C., Do Carmo S., Rassart E., Ganfornina M.D. Apolipoprotein D alters the early transcriptional response to oxidative stress in the adult cerebellum. J. Neurochem. 2011, 117:949-960.
4. Bishop R.E., Cambillau C., Privé G., Hsi D., Tillo D., Tillier E.R.M. Bacterial lipocalins: origin, structure and function. Lipocalins 2006, 28-40. Landes Biosciences, Georgetown, Texas. B. Akerstrom, N. Borregaard, D. Flower, J. Salier (Eds.).
5. Boyan G., Posser S., Ludwig P., Guntner M., Williams L. Ontogeny of identified cells from the median domain in the embryonic brain of the grasshopper Schistocerca gregaria. Arthropod Struct. Dev. 2004, 33:125-137.
6. Boyan G.S., Williams J.L. Embryonic development of the sensory innervation of the antenna of the grasshopper Schistocerca gregaria. Arthropod Struct. Dev. 2004, 33:381-397.
7. Boyan G.S., Williams J.L., Posser S., Braunig P. Morphological and molecular data argue for the labrum being non-apical, articulated, and the appendage of the intercalary segment in the locust. Arthropod Struct. Dev. 2002, 31:65-76.
8. Bunch T.A., Grinblat Y., Goldstein L.S. Characterization and use of the Drosophila metallothionein promoter in cultured Drosophila melanogaster cells. Nucleic Acids Res. 1988, 16:1043-1061.
9. Charron J.B., Sarhan F. Plant lipocalins. Lipocalins 2006, 41-48. Landes Biosciences, Georgetown, Texas. B. Akerstrom, N. Borregaard, D. Flower, J. Salier (Eds.).
10. Davis M.M., Primrose D.A., Hodgetts R.B. A member of the p38 mitogen-activated protein Kinase family is responsible for transcriptional induction of dopa decarboxylase in the epidermis of Drosophila melanogaster during the innate immune response. Mol. Cell Biol. 2008, 28:4883-4895.
11. de Magalhaes J.P., Curado J., Church G.M. Meta-analysis of age-related gene expression profiles identifies common signatures of aging. Bioinformatics 2009, 25:875-881.
12. Eisenhaber B., Bork P., Eisenhaber F. Prediction of potential GPI-modification sites in proprotein sequences. J. Mol. Biol. 1999, 292:741-758.
13. Filippov V., Filippova M., Kodrík D., Sehnal F. Two lipocalin-like peptides of insect brain. Mechanisms of Insect Metamorphosis and Diapause 1995, 35-43. Industrial Publishing & Consulting, Inc, Tokio, Japan. A. Suzuki, H. Kataoka, S., M (Eds.).
14. Flower D.R. The lipocalin protein family: structure and function. Biochem. J. 1996, 318:1-14.
15. Flower D.R., North A.C., Sansom C.E. The lipocalin protein family: structural and sequence overview. Biochim. Biophys. Acta 2000, 1482:9-24.
16. Foley B.R., Telonis-Scott M. Quantitative genetic analysis suggests causal association between cuticular hydrocarbon composition and desiccation survival in Drosophila melanogaster. Heredity (Edinb) 2011, 106:68-77.
17. Ganfornina M., Kayser H., Sanchez D. Lipocalins in Arthropoda: diversification and functional explorations. Lipocalins 2006, 40-74. Landes Bioscience, Georgetown, Texas. B. Akerstrom, N. Borregaard, D. Flower, J. Salier (Eds.).
18. Ganfornina M., Sanchez D., Greene L., Flower D.R. The Lipocalin protein family: protein sequence and structure. Lipocalins 2006, 17-27. Landes Bioscience, Georgetown, Texas. B. Akerstrom, N. Borregaard, D. Flower, J. Salier (Eds.).
19. Ganfornina M.D., Do Carmo S., Lora J.M., Torres-Schumann S., Vogel M., Allhorn M., González C., Bastiani M.J., Rassart E., Sanchez D. Apolipoprotein D is involved in the mechanisms regulating protection from oxidative stress. Aging Cell 2008, 7:506-515.
20. Ganfornina M.D., Do Carmo S., Martínez E., Tolivia J., Navarro A., Rassart E., Sanchez D. ApoD, a glia-derived apolipoprotein, is required for peripheral nerve functional integrity and a timely response to injury. Glia 2010, 58:1320-1334.
21. Ganfornina M.D., Gutierrez G., Bastiani M., Sanchez D. A phylogenetic analysis of the lipocalin protein family. Mol. Biol. Evol. 2000, 17:114-126.
22. Ganfornina M.D., Sanchez D., Bastiani M.J. Lazarillo, a new GPI-linked surface lipocalin, is restricted to a subset of neurons in the grasshopper embryo. Development 1995, 121:123-134.
23. Ganfornina M.D., Sanchez D., Bastiani M.J. Embryonic development of the enteric nervous system of the grasshopper Schistocerca americana. J. Comp. Neurol. 1996, 372:581-596.
24. Graf S., Ludwig P., Boyan G. Lazarillo expression reveals a subset of neurons contributing to the primary axon scaffold of the embryonic brain of the grasshopper Schistocerca gregaria. J. Comp. Neurol. 2000, 419:394-405.
25. Hull-Thompson J., Muffat J., Sanchez D., Walker D.W., Benzer S., Ganfornina M.D., Jasper H. Control of metabolic homeostasis by stress signaling is mediated by the lipocalin NLaz. PLoS Genet. 2009, 5:e1000460.
26. Hvidberg V., Jacobsen C., Strong R.K., Cowland J.B., Moestrup S.K., Borregaard N. The endocytic receptor megalin binds the iron transporting neutrophil-gelatinase-associated lipocalin with high affinity and mediates its cellular uptake. FEBS Lett. 2005, 579:773-777.
27. Ikeya T., Broughton S., Alic N., Grandison R., Partridge L. The endosymbiont Wolbachia increases insulin/IGF-like signalling in Drosophila. Proc. Biol. Sci. 2009, 276:3799-3807.
28. Jacobson J., Lambert A.J., Portero-Otin M., Pamplona R., Magwere T., Miwa S., Driege Y., Brand M.D., Partridge L. Biomarkers of aging in Drosophila. Aging Cell 2010, 9:466-477.
29. Kang Y., Ziegler R., van Antwerpen R., Law J.H. Characterization of the solubilized oocyte membrane receptor for insecticyanin, a biliprotein of the hawkmoth, Manduca sexta. Biochim. Biophys. Acta 1997, 1324:285-295.
30. Kawaguchi R., Yu J., Honda J., Hu J., Whitelegge J., Ping P., Wiita P., Bok D., Sun H. A membrane receptor for retinol binding protein mediates cellular uptake of vitamin A. Science 2007, 315:820-825.
31. Kim H.J., Je H.J., Cheon H.M., Kong S.Y., Han J., Yun C.Y., Han Y.S., Lee I.H., Kang Y.J., Seo S.J. Accumulation of 23 kDa lipocalin during brain development and injury in Hyphantria cunea. Insect Biochem. Mol. Biol. 2005, 35:1133-1141.
32. Kyte J., Doolittle R.F. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 1982, 157:105-132.
33. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
34. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
35. Loerch P.M., Lu T., Dakin K.A., Vann J.M., Isaacs A., Geula C., Wang J., Pan Y., Gabuzda D.H., Li C., Prolla T.A., Yankner B.A. Evolution of the aging brain transcriptome and synaptic regulation. PLoS ONE 2008, 3:e3329.
36. Marican C., Duportets L., Birman S., Jallon J.M. Female-specific regulation of cuticular hydrocarbon biosynthesis by dopamine in Drosophila melanogaster. Insect Biochem. Mol. Biol. 2004, 34:823-830.
37. Martins P.A., Gomes F., Vaz W.L., Moreno M.J. Binding of phospholipids to beta-Lactoglobulin and their transfer to lipid bilayers. Biochim. Biophys. Acta 2008, 1778:1308-1315.
38. Meunier N., Belgacem Y.H., Martin J.R. Regulation of feeding behaviour and locomotor activity by takeout in Drosophila. J. Exp. Biol. 2007, 210:1424-1434.
39. Muffat J., Walker D.W., Benzer S. Human ApoD, an apolipoprotein up-regulated in neurodegenerative diseases, extends lifespan and increases stress resistance in Drosophila. Proc. Natl. Acad. Sci. U S A 2008, 105:7088-7093.
40. Neckameyer W.S., Weinstein J.S. Stress affects dopaminergic signaling pathways in Drosophila melanogaster. Stress 2005, 8:117-131.
41. Nishi K., Sakai N., Komine Y., Maruyama T., Halsall H.B., Otagiri M. Structural and drug-binding properties of alpha(1)-acid glycoprotein in reverse micelles. Biochim. Biophys. Acta 2002, 1601:185-191.
42. Oudes A.J., Herr C.M., Olsen Y., Fleming J.E. Age-dependent accumulation of advanced glycation end-products in adult Drosophila melanogaster. Mech. Ageing Dev. 1998, 100:221-229.
43. Riddiford L.M., Palli S.R., Hiruma K., Li W., Green J., Hice R.H., Wolfgang W.J., Webb B.A. Developmental expression, synthesis, and secretion of insecticyanin by the epidermis of the tobacco hornworm, Manduca sexta. Arch. Insect Biochem. Physiol. 1990, 14:171-190.
44. Rong Y.S., Titen S.W., Xie H.B., Golic M.M., Bastiani M., Bandyopadhyay P., Olivera B.M., Brodsky M., Rubin G.M., Golic K.G. Targeted mutagenesis by homologous recombination in D. melanogaster. Genes Dev. 2002, 16:1568-1581.
45. Rouault J.D., Marican C., Wicker-Thomas C., Jallon J.M. Relations between cuticular hydrocarbon (HC) polymorphism, resistance against desiccation and breeding temperature; a model for HC evolution in D. melanogaster and D. simulans. Genetica 2004, 120:195-212.
46. Ruiz M., Sanchez D., Canal I., Acebes A., Ganfornina M.D. Sex-dependent modulation of longevity by two Drosophila homologues of human Apolipoprotein D, GLaz and NLaz. Exp. Gerontol. 2011, 46:579-589.
47. Saaren-Seppala H., Jauhiainen M., Tervo T.M., Redl B., Kinnunen P.K., Holopainen J.M. Interaction of purified tear lipocalin with lipid membranes. Invest. Ophthalmol. Vis. Sci. 2005, 46:3649-3656.
48. Saito H. Purification and characterization of two insecticyanin-type proteins from the larval hemolymph of the Eri-silkworm, Samia cynthia ricini. Biochim. Biophys. Acta 1998, 1380:141-150.
49. Sakai M., Wu C., Suzuki K. Nucleotide and deduced amino acid sequences of a cDNA encoding a Lipocalin protein in the central nervous system of Bombys mori. Nippon Sanshi-gaku Zasshi 2001, 70:105-111.
50. Sanchez D., Ganfornina M.D., Bastiani M.J. Developmental expression of the lipocalin Lazarillo and its role in axonal pathfinding in the grasshopper embryo. Development 1995, 121:135-147.
51. Sanchez D., Ganfornina M.D., Bastiani M.J. Lazarillo, a neuronal lipocalin in grasshoppers with a role in axon guidance. Biochim. Biophys. Acta 2000, 1482:102-109.
52. Sanchez D., Ganfornina M.D., Gutierrez G., Gauthier-Janeau A.C., Risler J.L., Salier J. Lipocalin genes and their evolutionary history. Lipocalins 2006, 5-16. Landes Biosciences, Georgetown, Texas. B. Akerström, N. Borregaard, D. Flover, J. Salier (Eds.).
53. Sanchez D., Ganfornina M.D., Gutiérrez G., Marín A. Exon-intron structure and evolution of the lipocalin gene family. Mol. Biol. Evol. 2003, 20:775-783.
54. Sanchez D., Ganfornina M.D., Torres-Schumann S., Speese S.D., Lora J.M., Bastiani M.J. Characterization of two novel lipocalins expressed in the Drosophila embryonic nervous system. Int. J. Dev. Biol. 2000, 44:349-360.
55. Sanchez D., Lopez-Arias B., Torroja L., Canal I., Wang X., Bastiani M.J., Ganfornina M.D. Loss of glial lazarillo, a homolog of apolipoprotein D, reduces lifespan and stress resistance in Drosophila. Curr. Biol. 2006, 16:680-686.
56. Sanchez D., Ortega-Cubero S., åkerström B., Herrera M., Bastiani M.J., Ganfornina M.D. Molecular interactions of the neuronal GPI-anchored lipocalin Lazarillo. J. Mol. Recognit. 2008, 21:313-323.
57. Schmidt F.S., Skerra A. The bilin-binding protein of Pieris brassicae. cDNA sequence and regulation of expression reveal distinct features of this insect pigment protein. Eur. J. Biochem. 1994, 219:855-863.
58. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protocol. 2008, 3:1101-1108.
59. Scholnick S.B., Morgan B.A., Hirsh J. The cloned dopa decarboxylase gene is developmentally regulated when reintegrated into the Drosophila genome. Cell 1983, 34:37-45.
60. Sehringer B., Kayser H. Butterfly wings, a new site of porphyrin synthesis and cleavage: studies on the expression of the lipocalin bilin-binding protein in Pieris brassicae. Insect Biochem. Mol. Biol. 2006, 36:482-491.
61. Sekine Y., Takagahara S., Hatanaka R., Watanabe T., Oguchi H., Noguchi T., Naguro I., Kobayashi K., Tsunoda M., Funatsu T., Nomura H., Toyoda T., Matsuki N., Kuranaga E., Miura M., Takeda K., Ichijo H. p38 MAPKs regulate the expression of genes in the dopamine synthesis pathway through phosphorylation of NR4A nuclear receptors. J. Cell Sci. 2011, 124:3006-3016.
62. Van Dijk W., Do Carmo S., Rassart E., Dahlbäck B., Sodetz J. The plasma lipocalins alpha1-acid-glycoprotein, apolipoprotein D, apolipoprotein M and complement protein 8gamma. Lipocalins 2006, 140-166. Landes Bioscience, Georgetown, Texas. B. Akerström, N. Borregaard, D. Flover, J. Salier (Eds.).
63. Walker D.W., Muffat J., Rundel C., Benzer S. Overexpression of a Drosophila homolog of apolipoprotein D leads to increased stress resistance and extended lifespan. Curr. Biol. 2006, 16:674-679.
64. Wang D., Marsh J.L., Ayala F.J. Evolutionary changes in the expression pattern of a developmentally essential gene in three Drosophila species. Proc. Natl. Acad. Sci. U S A 1996, 93:7103-7107.
65. Wicker-Thomas C., Guenachi I., Keita Y.F. Contribution of oenocytes and pheromones to courtship behaviour in Drosophila. BMC Biochem. 2009, 10:21.
66. Wicker-Thomas C., Hamann M. Interaction of dopamine, female pheromones, locomotion and sex behavior in Drosophila melanogaster. J. Insect Physiol. 2008, 54:1423-1431.
67. Wojnar P., Lechner M., Merschak P., Redl B. Molecular cloning of a novel lipocalin-1 interacting human cell membrane receptor using phage display. J. Biol. Chem. 2001, 276:20206-20212.
68. Zeng C., Spielman A.I., Vowels B.R., Leyden J.J., Biemann K., Preti G. A human axillary odorant is carried by apolipoprotein D. Proc. Natl. Acad. Sci. U S A 1996, 93:6626-6630.