Individual carboxypeptidase D domains have both redundant and unique functions in Drosophila development and behavior

Cellular and Molecular Life Sciences

Volumn 67, Issue 17, 2010, Pages 2991-3004

  Sidyelyeva, Galyna ^a   Wegener, Christian ^b   Schoenfeld, Brian P ^a   Bell, Aaron J ^a   Baker, Nicholas E ^a   McBride, Sean M J ^a   Fricker, Lloyd D ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Carboxypeptidase; Neuropeptide; Peptidase; Peptide processing; Protease

Indexed keywords

ADIPOKINETIC HORMONE; CARBOXYPEPTIDASE D; METALLOCARBOXYPEPTIDASE D; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; PROTEIN;

ALCOHOL TOLERANCE; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COLD SENSITIVITY; CONTROLLED STUDY; DROSOPHILA; EMBRYO; FEMALE; INSECT DEVELOPMENT; LONG TERM MEMORY; MALE; MEMORY DISORDER; NONHUMAN; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; TRANSGENE; TRANSGENIC ANIMAL; WILD TYPE; ALTERNATIVE RNA SPLICING; ANATOMY AND HISTOLOGY; ANIMAL; FORELIMB; GENE STRUCTURE; GENETICS; MASS SPECTROMETRY; MEMORY; PHENOTYPE; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ALTERNATIVE SPLICING; ANIMALS; ANIMALS, GENETICALLY MODIFIED; DROSOPHILA; DROSOPHILA PROTEINS; GENE COMPONENTS; MEMORY; PHENOTYPE; PROTEIN STRUCTURE, TERTIARY; PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; WING;

EID: 77956777446     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-010-0369-8     Document Type: Article

References (70)

1. PH Taghert JA Veenstra 2003 Drosophila neuropeptide signaling Adv Genet 49 1 65 10.1016/S0065-2660(03)01001-0 1:CAS:528:DC%2BD3sXltV2gsLw%3D 12779250 (Pubitemid 137639211)
2. FL Strand 2003 Neuropeptides: general characteristics and neuropharmaceutical potential in treating CNS disorders Prog Drug Res 61 1 37 1:CAS:528:DC%2BD3sXpvFert7k%3D 14674607
3. LD Fricker 2005 Neuropeptide-processing enzymes: applications for drug discovery AAPS J 7 E449 E455 10.1208/aapsj070244 1:CAS:528:DC%2BD2MXht1ylt7bE 16353923 (Pubitemid 43071330)
4. Y Rouille SJ Duguay K Lund M Furuta Q Gong G Lipkind AA Oliva Jr SJ Chan DF Steiner 1995 Proteolytic processing mechanisms in the biosynthesis of neuroendocrine peptides: the subtilisin-like proprotein convertases Front Neuroendocrinol 16 322 361 10.1006/frne.1995.1012 1:CAS:528:DyaK2MXpvFyqsbw%3D 8557169
5. DF Steiner 1998 The proprotein convertases Curr Opin Chem Biol 2 31 39 10.1016/S1367-5931(98)80033-1 1:CAS:528:DyaK1cXitFygsbs%3D 9667917
6. M Han D Park PJ Vanderzalm RE Mains BA Eipper PH Taghert 2004 Drosophila uses two distinct neuropeptide amidating enzymes, dPAL1 and dPAL2 J Neurochem 90 129 141 10.1111/j.1471-4159.2004.02464.x 1:CAS:528:DC%2BD2cXlvFKls7Y%3D 15198673 (Pubitemid 38879168)
7. PH Taghert RS Hewes JH Park MA O'Brien M Han ME Peck 2001 Multiple amidated neuropeptides are required for normal circadian locomotor rhythms in Drosophila J Neurosci 21 6673 6686 1:CAS:528:DC%2BD3MXmt1Wju7Y%3D 11517257
8. JL Arolas J Vendrell FX Aviles LD Fricker 2007 Metallocarboxypeptidases: emerging drug targets in biomedicine Curr Pharm Des 13 349 366 10.2174/138161207780162980 1:CAS:528:DC%2BD2sXjvVyltro%3D 17311554 (Pubitemid 46477758)
9. A Fernandez-Gonzalez AR La Spada J Treadaway JC Higdon BS Harris RL Sidman JI Morgan J Zuo 2002 Purkinje cell degeneration (PCD) phenotypes caused by mutations in the axotomy-induced gene, Nna1 Science 295 1904 1906 10.1126/science.1068912 1:CAS:528:DC%2BD38XhvFCltLg%3D 11884758 (Pubitemid 34214129)
10. A Harris JI Morgan M Pecot A Soumare A Osborne HD Soares 2000 Regenerating motor neurons express Nna1, a novel ATP/GTP-binding protein related to zinc carboxypeptidases Mol Cell Neurosci 16 578 596 10.1006/mcne.2000.0900 1:CAS:528:DC%2BD3cXotFWgsbo%3D 11083920 (Pubitemid 32001307)
11. E Kalinina R Biswas I Berezniuk A Hermoso FX Aviles LD Fricker 2007 A novel subfamily of mouse cytosolic carboxypeptidases FASEB J 21 836 850 10.1096/fj.06-7329com 1:CAS:528:DC%2BD2sXis1ehsL0%3D 17244818 (Pubitemid 46348257)
12. Rodriguez de la Vega M, Sevilla RG, Hermoso A, Lorenzo J, Tanco S, Diez A, Fricker LD, Bautista JM, Aviles FX (2007) Nna1-like proteins are active metallocarboxypeptidases of a new and diverse M14 subfamily. FASEB J 21:851-865
13. SE Reznik LD Fricker 2001 Carboxypeptidases from A to Z: implications in embryonic development and Wnt binding Cell Mol Life Sci 58 1790 1804 10.1007/PL00000819 1:CAS:528:DC%2BD3MXovVygurg%3D 11766880
14. T Ishikawa K Murakami Y Kido S Ohnishi Y Yazaki F Harada K Kuroki 1998 Cloning, functional expression, and chromosomal localization of the human and mouse gp180-carboxypeptidase D-like enzyme Gene 215 361 370 10.1016/S0378- 1119(98)00270-4 1:CAS:528:DyaK1cXlvFShurY%3D 9714835 (Pubitemid 28382939)
15. K Kuroki F Eng T Ishikawa C Turck F Harada D Ganem 1995 gp180, a host cell glycoprotein that binds duck hepatitis B virus particles, is encoded by a member of the carboxypeptidase gene family J Biol Chem 270 15022 15028 10.1074/jbc.270.25.15022 1:CAS:528:DyaK2MXmsFKqsb4%3D 7797483
16. F Tan M Rehli SW Krause RA Skidgel 1997 Sequence of human carboxypeptidase D reveals it to be a member of the regulatory carboxypeptidase family with three tandem active site domains Biochem J 327 Pt 1 81 87 1:CAS:528:DyaK2sXmvVGrtr0%3D 9355738
17. X Xin O Varlamov R Day W Dong MM Bridgett EH Leiter LD Fricker 1997 Cloning and sequence analysis of cDNA encoding rat carboxypeptidase D DNA Cell Biol 16 897 909 10.1089/dna.1997.16.897 1:CAS:528:DyaK2sXltFGktr0%3D 9260933
18. FJ Eng EG Novikova K Kuroki D Ganem LD Fricker 1998 gp180, a protein that binds duck hepatitis B virus particles, has metallocarboxypeptidase D-like enzymatic activity J Biol Chem 273 8382 8388 10.1074/jbc.273.14.8382 1:CAS:528:DyaK1cXitlOhs7c%3D 9525948 (Pubitemid 28168899)
19. EG Novikova FJ Eng L Yan Y Qian LD Fricker 1999 Characterization of the enzymatic properties of the first and second domains of metallocarboxypeptidase D J Biol Chem 274 28887 28892 10.1074/jbc.274.41.28887 1:CAS:528: DyaK1MXmslWqsL4%3D 10506132 (Pubitemid 29477041)
20. G Sidyelyeva LD Fricker 2002 Characterization of Drosophila carboxypeptidase D J Biol Chem 277 49613 49620 10.1074/jbc.M209652200 1:CAS:528:DC%2BD38XpsFaksbk%3D 12393882 (Pubitemid 36014402)
21. G Sidyelyeva NE Baker LD Fricker 2006 Characterization of the molecular basis of the Drosophila mutations in carboxypeptidase D Effect on enzyme activity and expression J Biol Chem 281 13844 13852 10.1074/jbc.M513499200 1:CAS:528:DC%2BD28Xkt1ymu74%3D 16556608 (Pubitemid 43855300)
22. SH Settle Jr MM Green KC Burtis 1995 The silver gene of Drosophila melanogaster encodes multiple carboxypeptidases similar to mammalian prohormone-processing enzymes Proc Natl Acad Sci USA 92 9470 9474 10.1073/pnas.92.21.9470 1:CAS:528:DyaK2MXoslCntbk%3D 7568156
23. S Tweedie M Ashburner K Falls P Leyland P McQuilton S Marygold G Millburn D Osumi-Sutherland A Schroeder R Seal H Zhang 2009 FlyBase: enhancing Drosophila gene ontology annotations Nucleic Acids Res 37 D555 D559 10.1093/nar/gkn788 1:CAS:528:DC%2BD1cXhsFejtLnN 18948289
24. HM Bourbon G Gonzy-Treboul F Peronnet MF Alin C Ardourel C Benassayag D Cribbs J Deutsch P Ferrer M Haenlin JA Lepesant S Noselli A Vincent 2002 A P-insertion screen identifying novel X-linked essential genes in Drosophila Mech Dev 110 71 83 10.1016/S0925-4773(01)00566-4 1:CAS:528:DC%2BD3MXovF2htr4%3D 11744370
25. AH Brand N Perrimon 1993 Targeted gene expression as a means of altering cell fates and generating dominant phenotypes Development 118 401 415 1:CAS:528:DyaK3sXlvFKrt7w%3D 8223268
26. RC Rayne M O'Shea 1994 Reconstitution of adipokinetic hormone biosynthesis in vitro indicates steps in prohormone processing Eur J Biochem 219 781 789 10.1111/j.1432-1033.1994.tb18558.x 1:CAS:528:DyaK2cXis1eqs7c%3D 8112329
27. R Predel C Wegener WK Russell SE Tichy DH Russell RJ Nachman 2004 Peptidomics of CNS-associated neurohemal systems of adult Drosophila melanogaster: a mass spectrometric survey of peptides from individual flies J Comp Neurol 474 379 392 10.1002/cne.20145 1:CAS:528:DC%2BD2cXlsFCmsLo%3D 15174081 (Pubitemid 38724145)
28. C Wegener T Reinl L Jansch R Predel 2006 Direct mass spectrometric peptide profiling and fragmentation of larval peptide hormone release sites in Drosophila melanogaster reveals tagma-specific peptide expression and differential processing J Neurochem 96 1362 1374 10.1111/j.1471-4159.2005.03634. x 1:CAS:528:DC%2BD28XivFSrurk%3D 16441518
29. G Lee JH Park 2004 Hemolymph sugar homeostasis and starvation-induced hyperactivity affected by genetic manipulations of the adipokinetic hormone-encoding gene in Drosophila melanogaster Genetics 167 311 323 10.1534/genetics.167.1.311 1:CAS:528:DC%2BD2cXlsFOitrk%3D 15166157 (Pubitemid 38736390)
30. T Wen CA Parrish D Xu Q Wu P Shen 2005 Drosophila neuropeptide F and its receptor, NPFR1, define a signaling pathway that acutely modulates alcohol sensitivity Proc Natl Acad Sci USA 102 2141 2146 10.1073/pnas.0406814102 1:CAS:528:DC%2BD2MXhvFGqs7w%3D 15677721 (Pubitemid 40262025)
31. SJ Broughton MD Piper T Ikeya TM Bass J Jacobson Y Driege P Martinez E Hafen DJ Withers SJ Leevers L Partridge 2005 Longer lifespan, altered metabolism, and stress resistance in Drosophila from ablation of cells making insulin-like ligands Proc Natl Acad Sci USA 102 3105 3110 10.1073/pnas. 0405775102 1:CAS:528:DC%2BD2MXitVSktbs%3D 15708981 (Pubitemid 40299923)
32. SM McBride CH Choi Y Wang D Liebelt E Braunstein D Ferreiro A Sehgal KK Siwicki TC Dockendorff HT Nguyen TV McDonald TA Jongens 2005 Pharmacological rescue of synaptic plasticity, courtship behavior, and mushroom body defects in a Drosophila model of fragile X syndrome Neuron 45 753 764 10.1016/j.neuron. 2005.01.038 1:CAS:528:DC%2BD2MXis1yrsL8%3D 15748850 (Pubitemid 40320709)
33. SM McBride G Giuliani C Choi P Krause D Correale K Watson G Baker KK Siwicki 1999 Mushroom body ablation impairs short-term memory and long-term memory of courtship conditioning in Drosophila melanogaster Neuron 24 967 977 10.1016/S0896-6273(00)81043-0 1:CAS:528:DC%2BD3cXislaltA%3D%3D 10624959
34. RW Siegel JC Hall 1979 Conditioned responses in courtship behavior of normal and mutant Drosophila Proc Natl Acad Sci USA 76 3430 3434 10.1073/pnas.76.7.3430 1:STN:280:DC%2BC3cngsl2jtA%3D%3D 16592682 (Pubitemid 9233974)
35. D Wang L Qian H Xiong J Liu WS Neckameyer S Oldham K Xia J Wang R Bodmer Z Zhang 2006 Antioxidants protect PINK1-dependent dopaminergic neurons in Drosophila Proc Natl Acad Sci USA 103 13520 13525 10.1073/pnas.0604661103 1:CAS:528:DC%2BD28XpvVeqt7o%3D 16938835 (Pubitemid 44380140)
36. C Wegener S Neupert R Predel 2010 Direct MALDI-TOF mass spectrometric peptide profiling of neuroendocrine tissue of Drosophila Methods Mol Biol 615 117 127 10.1007/978-1-60761-535-4-9 1:CAS:528:DC%2BC3cXnvFGqtrw%3D 20013204
37. AH Brand AS Manoukian N Perrimon 1994 Ectopic expression in Drosophila Methods Cell Biol 44 635 654 10.1016/S0091-679X(08)60936-X 1:CAS:528: DyaK2MXktlarsbg%3D 7707973
38. O Varlamov LD Fricker 1998 Intracellular trafficking of metallocarboxypeptidase D in AtT-20 cells: localization to the trans-Golgi network and recycling from the cell surface J Cell Sci 111 Pt 7 877 885 1:CAS:528:DyaK1cXivV2htLw%3D 9490632
39. SS Vembar JL Brodsky 2008 One step at a time: endoplasmic reticulum-associated degradation Nat Rev Mol Cell Biol 9 944 957 10.1038/nrm2546 1:CAS:528:DC%2BD1cXhsVWhurjI 19002207
40. O Varlamov FJ Eng EG Novikova LD Fricker 1999 Localization of metallocarboxypeptidase D in AtT-20 cells. Potential role in prohormone processing J Biol Chem 274 14759 14767 10.1074/jbc.274.21.14759 1:CAS:528:DyaK1MXks1Kqs70%3D 10329672 (Pubitemid 29265856)
41. Fricker LD (1998) Metallocarboxypeptidase D. In: Barrett AJ, Rawlings ND, Woessner JF (eds) Handbook of proteolytic enzymes, 1st edn. Academic Press, San Diego, pp 1349-1351
42. SS Blair 2007 Wing vein patterning in Drosophila and the analysis of intercellular signaling Annu Rev Cell Dev Biol 23 293 319 10.1146/annurev. cellbio.23.090506.123606 1:CAS:528:DC%2BD2sXhtlartr3I 17506700
43. Fricker LD (1998) Carboxypeptidase E/H. In: Barrett AJ, Rawlings ND, Woessner JF (eds) Handbook of proteolytic enzymes, 1st edn. Academic Press, San Diego, pp 1341-1344
44. MS Moore J DeZazzo AY Luk T Tully CM Singh U Heberlein 1998 Ethanol intoxication in Drosophila: genetic and pharmacological evidence for regulation by the cAMP signaling pathway Cell 93 997 1007 10.1016/S0092-8674(00)81205-2 1:CAS:528:DyaK1cXjvFKqsLk%3D 9635429 (Pubitemid 28280793)
45. L Tompkins RW Siegel DA Gailey JC Hall 1983 Conditioned courtship in Drosophila and its mediation by association of chemical cues Behav Genet 13 565 578 10.1007/BF01076402 1:STN:280:DyaL2c7ltlOhtg%3D%3D 6422921
46. JF Riordan 2003 Angiotensin-I-converting enzyme and its relatives Genome Biol 4 225 10.1186/gb-2003-4-8-225 12914653 (Pubitemid 37039111)
47. RJ Siviter RJ Nachman MP Dani JN Keen AD Shirras RE Isaac 2002 Peptidyl dipeptidases (Ance and Acer) of Drosophila melanogaster: major differences in the substrate specificity of two homologs of human angiotensin I-converting enzyme Peptides 23 2025 2034 10.1016/S0196-9781(02)00190-0 1:CAS:528: DC%2BD38XosFKrsrY%3D 12431741 (Pubitemid 35341612)
48. S Cal V Quesada C Garabaya C Lopez-Otin 2003 Polyserase-I, a human polyprotease with the ability to generate independent serine protease domains from a single translation product Proc Natl Acad Sci USA 100 9185 9190 10.1073/pnas.1633392100 1:CAS:528:DC%2BD3sXmtlyksbg%3D 12886014 (Pubitemid 37033904)
49. S Cal A Moncada-Pazos C Lopez-Otin 2007 Expanding the complexity of the human degradome: polyserases and their tandem serine protease domains Front Biosci 12 4661 4669 10.2741/2415 1:CAS:528:DC%2BD2sXms1Klt7o%3D 17485402
50. F Schweisguth 2004 Regulation of notch signaling activity Curr Biol 14 R129 R138 1:CAS:528:DC%2BD2cXhtFChtr4%3D 14986688
51. BL Hogan 1996 Bone morphogenetic proteins in development Curr Opin Genet Dev 6 432 438 10.1016/S0959-437X(96)80064-5 1:CAS:528:DyaK28Xlt1Kmtrk%3D 8791534 (Pubitemid 26280795)
52. RP Ray KA Wharton 2001 Context-dependent relationships between the BMPs gbb and dpp during development of the Drosophila wing imaginal disk Development 128 3913 3925 1:CAS:528:DC%2BD3MXotFGksb0%3D 11641216
53. Y Cui F Jean G Thomas JL Christian 1998 BMP-4 is proteolytically activated by furin and/or PC6 during vertebrate embryonic development EMBO J 17 4735 4743 10.1093/emboj/17.16.4735 1:CAS:528:DyaK1cXlslOhtLk%3D 9707432 (Pubitemid 28377173)
54. T Nakayama Y Cui JL Christian 2000 Regulation of BMP/Dpp signaling during embryonic development Cell Mol Life Sci 57 943 956 10.1007/PL00000736 1:CAS:528:DC%2BD3cXlsl2gs74%3D 10950309
55. C Degnin F Jean G Thomas JL Christian 2004 Cleavages within the prodomain direct intracellular trafficking and degradation of mature bone morphogenetic protein-4 Mol Biol Cell 15 5012 5020 10.1091/mbc.E04-08-0673 1:CAS:528:DC%2BD2cXpslKnsL8%3D 15356272 (Pubitemid 39392215)
56. E Bier 2000 Drawing lines in the Drosophila wing: initiation of wing vein development Curr Opin Genet Dev 10 393 398 10.1016/S0959-437X(00)00102-7 1:CAS:528:DC%2BD3cXlt1Sjtbk%3D 10889058 (Pubitemid 30450042)
57. JF De Celis 2003 Pattern formation in the Drosophila wing: the development of the veins Bioessays 25 443 451 10.1002/bies.10258 12717815 (Pubitemid 36565682)
58. CA Conley R Silburn MA Singer A Ralston D Rohwer-Nutter DJ Olson W Gelbart SS Blair 2000 Crossveinless 2 contains cysteine-rich domains and is required for high levels of BMP-like activity during the formation of the cross veins in Drosophila Development 127 3947 3959 1:CAS:528:DC%2BD3cXnslGrt7g%3D 10952893
59. J Lewis 2008 From signals to patterns: space, time, and mathematics in developmental biology Science 322 399 403 10.1126/science.1166154 1:CAS:528:DC%2BD1cXht1CitrvE 18927385
60. S Waddell JD Armstrong T Kitamoto K Kaiser WG Quinn 2000 The amnesiac gene product is expressed in two neurons in the Drosophila brain that are critical for memory Cell 103 805 813 10.1016/S0092-8674(00)00183-5 1:CAS:528:DC%2BD3cXos1Snu7g%3D 11114336
61. KH Berger EC Kong J Dubnau T Tully MS Moore U Heberlein 2008 Ethanol sensitivity and tolerance in long-term memory mutants of Drosophila melanogaster Alcohol Clin Exp Res 32 895 908 10.1111/j.1530-0277.2008.00659.x 1:CAS:528:DC%2BD1cXmvVShtbg%3D 18435628 (Pubitemid 351589401)
62. J Dubnau AS Chiang L Grady J Barditch S Gossweiler J McNeil P Smith F Buldoc R Scott U Certa C Broger T Tully 2003 The staufen/pumilio pathway is involved in Drosophila long-term memory Curr Biol 13 286 296 10.1016/S0960-9822(03)00064-2 1:CAS:528:DC%2BD3sXhsValt7Y%3D 12593794 (Pubitemid 36230019)
63. C Wegener A Gorbashov 2008 Molecular evolution of neuropeptides in the genus Drosophila Genome Biol 9 R131 10.1186/gb-2008-9-8-r131 18717992
64. G Baggerman K Boonen P Verleyen A De Loof L Schoofs 2005 Peptidomic analysis of the larval Drosophila melanogaster central nervous system by two-dimensional capillary liquid chromatography quadrupole time-of-flight mass spectrometry J Mass Spectrom 40 250 260 10.1002/jms.744 1:CAS:528: DC%2BD2MXitFyhurs%3D 15706625 (Pubitemid 40327264)
65. AB Corl AR Rodan U Heberlein 2005 Insulin signaling in the nervous system regulates ethanol intoxication in Drosophila melanogaster Nat Neurosci 8 18 19 10.1038/nn1363 1:CAS:528:DC%2BD2MXhtFWgsg%3D%3D 15592467 (Pubitemid 41236724)
66. AR Rodan JA Kiger Jr U Heberlein 2002 Functional dissection of neuroanatomical loci regulating ethanol sensitivity in Drosophila J Neurosci 22 9490 9501 1:CAS:528:DC%2BD3sXmsVGmsrc%3D 12417673
67. EJ Rulifson SK Kim R Nusse 2002 Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes Science 296 1118 1120 10.1126/science. 1070058 1:CAS:528:DC%2BD38XjslamsLo%3D 12004130 (Pubitemid 34517128)
68. MB Feany WG Quinn 1995 A neuropeptide gene defined by the Drosophila memory mutant amnesiac Science 268 869 873 10.1126/science.7754370 1:CAS:528:DyaK2MXls1Sgs7c%3D 7754370
69. D Coates RE Isaac J Cotton R Siviter TA Williams A Shirras P Corvol V Dive 2000 Functional conservation of the active sites of human and Drosophila angiotensin I-converting enzyme Biochemistry 39 8963 8969 10.1021/bi000593q 1:CAS:528:DC%2BD3cXksFaqsrY%3D 10913309 (Pubitemid 30602807)
70. M Hayama Y Okumura E Takahashi A Shimabukuro M Tamura N Takeda T Kubo H Kido 2007 Identification and analysis of the promoter region of the type II transmembrane serine protease polyserase-1 and its transcript variants Biol Chem 388 853 858 10.1515/BC.2007.093 1:CAS:528:DC%2BD2sXovFansb4%3D 17655505 (Pubitemid 47184844)