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Isolation of secreted proteins from Drosophila ovaries and embryos through in vivo BirA-mediated biotinylation


Autoři: Leslie M. Stevens aff001;  Yuan Zhang aff002;  Yuri Volnov aff001;  Geng Chen aff001;  David S. Stein aff001
Působiště autorů: Department of Molecular Biosciences, Institute for Cellular and Molecular Biology, The University of Texas at Austin, Austin, Texas, United States of America aff001;  Section of Molecular Cell and Developmental Biology, Institute for Cellular and Molecular Biology, The University of Texas at Austin, Austin, Texas, United States of America aff002
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0219878

Souhrn

The extraordinarily strong non-covalent interaction between biotin and avidin (kD = 10−14–10−16) has permitted this interaction to be used in a wide variety of experimental contexts. The Biotin Acceptor Peptide (BAP), a 15 amino acid motif that can be biotinylated by the E. coli BirA protein, has been fused to proteins-of-interest, making them substrates for in vivo biotinylation. Here we report on the construction and characterization of a modified BirA bearing signals for secretion and endoplasmic reticulum (ER) retention, for use in experimental contexts requiring biotinylation of secreted proteins. When expressed in the Drosophila female germline or ovarian follicle cells under Gal4-mediated transcriptional control, the modified BirA protein could be detected and shown to be enzymatically active in ovaries and progeny embryos. Surprisingly, however, it was not efficiently retained in the ER, and instead appeared to be secreted. To determine whether this secreted protein, now designated secBirA, could biotinylate secreted proteins, we generated BAP-tagged versions of two secreted Drosophila proteins, Torsolike (Tsl) and Gastrulation Defective (GD), which are normally expressed maternally and participate in embryonic pattern formation. Both Tsl-BAP and GD-BAP were shown to exhibit normal patterning activity. Co-expression of Tsl-BAP together with secBirA in ovarian follicle cells resulted in its biotinylation, which permitted its isolation from both ovaries and progeny embryos using Avidin-coupled affinity matrix. In contrast, co-expression with secBirA in the female germline did not result in detectable biotinylation of GD-BAP, possibly because the C-terminal location of the BAP tag made it inaccessible to BirA in vivo. Our results indicate that secBirA directs biotinylation of proteins bound for secretion in vivo, providing access to powerful experimental approaches for secreted proteins-of-interest. However, efficient biotinylation of target proteins may vary depending upon the location of the BAP tag or other structural features of the protein.

Klíčová slova:

Drosophila melanogaster – Embryos – Endoplasmic reticulum – Ovaries – Protein extraction – Protein interactions – Biotinylation – Biotin


Zdroje

1. Casadaban MJ. Fusion of the Escherichia coli lac genes to the ara promoter: a general technique using bacteriophage Mu-1 insertions. Proceedings of the National Academy of Sciences. 1975 Mar 1;72(3):809–13.

2. Casadaban MJ. Regulation of the regulatory gene for the arabinose pathway, araC. Journal of molecular biology. 1976 Jul 5;104(3):557–66. doi: 10.1016/0022-2836(76)90120-0 781294

3. Casadaban MJ. Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. Journal of molecular biology. 1976 Jul 5;104(3):541–55. doi: 10.1016/0022-2836(76)90119-4 781293

4. Silhavy TJ, Casadaban MJ, Shuman HA, Beckwith JR. Conversion of beta-galactosidase to a membrane-bound state by gene fusion. Proceedings of the National Academy of Sciences. 1976 Oct 1;73(10):3423–7.

5. Casadaban MJ, Cohen SN. Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. Journal of molecular biology. 1980 Apr 5;138(2):179–207. doi: 10.1016/0022-2836(80)90283-1 6997493

6. Shimomura O, Johnson FH, Saiga Y. Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan, Aequorea. Journal of cellular and comparative physiology. 1962 Jun;59(3):223–39.

7. Prasher DC, Eckenrode VK, Ward WW, Prendergast FG, Cormier MJ. Primary structure of the Aequorea victoria green-fluorescent protein. Gene. 1992 Feb 15;111(2):229–33. doi: 10.1016/0378-1119(92)90691-h 1347277

8. Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC. Green fluorescent protein as a marker for gene expression. Science. 1994 Feb 11;263(5148):802–5. doi: 10.1126/science.8303295 8303295

9. Heim R, Prasher DC, Tsien RY. Wavelength mutations and posttranslational autoxidation of green fluorescent protein. Proceedings of the National Academy of Sciences. 1994 Dec 20;91(26):12501–4.

10. Smith DB, Johnson KS. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene. 1988 Jul 15;67(1):31–40. doi: 10.1016/0378-1119(88)90005-4 3047011

11. Bedouelle H, Duplay P, Hofnung M. Expression, export and one-step purification of proteins by fusion to the MalE protein of E. coli. Comptes rendus de l'Academie des sciences. Serie III, Sciences de la vie. 1987;305(17):623–6.

12. Bedouelle H, Duplay P. Production in Escherichia coli and one‐step purification of bifunctional hybrid proteins which bind maltose: Export of the Klenow polymerase into the periplasmic space. European journal of biochemistry. 1988 Feb;171(3):541–9. doi: 10.1111/j.1432-1033.1988.tb13823.x 3278900

13. di Guana C, Lib P, Riggsa PD, Inouyeb H. Vectors that facilitate the expression and purification of foreign peptides in Escherichia coli by fusion to maltose-binding protein. Gene. 1988 Jul 15;67(1):21–30. doi: 10.1016/0378-1119(88)90004-2 2843437

14. Maina CV, Riggs PD, Grandea III AG, Slatko BE, Moran LS, Tagliamonte JA, et al. An Escherichia coli vector to express and purify foreign proteins by fusion to and separation from maltose-binding protein. Gene. 1988 Dec 30;74(2):365–73. doi: 10.1016/0378-1119(88)90170-9 3073105

15. Wilson IA, Niman HL, Houghten RA, Cherenson AR, Connolly ML, Lerner RA. The structure of an antigenic determinant in a protein. Cell. 1984 Jul 1;37(3):767–78. doi: 10.1016/0092-8674(84)90412-4 6204768

16. Evan GI, Lewis GK, Ramsay G, Bishop JM. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Molecular and cellular biology. 1985 Dec 1;5(12):3610–6. doi: 10.1128/mcb.5.12.3610 3915782

17. Hopp TP, Prickett KS, Price VL, Libby RT, March CJ, Cerretti DP, et al. A short polypeptide marker sequence useful for recombinant protein identification and purification. Bio/technology. 1988 Oct;6(10):1204.

18. Keefe AD, Wilson DS, Seelig B, Szostak JW. One-step purification of recombinant proteins using a nanomolar-affinity streptavidin-binding peptide, the SBP-Tag. Protein expression and purification. 2001 Dec 1;23(3):440–6. doi: 10.1006/prep.2001.1515 11722181

19. Schmidt TG, Skerra A. The random peptide library-assisted engineering of a C-terminal affinity peptide, useful for the detection and purification of a functional Ig Fv fragment. Protein Engineering, Design and Selection. 1993 Jan 1;6(1):109–22.

20. Skerra A, Schmidt TG. Use of the Strep-tag and streptavidin for detection and purification of recombinant proteins. In: Thorner J, Emr S, Abelson J, editors. Methods in enzymology, Volume 326. Applications of chimeric genes and hybrid proteins, Part A: Gene expression and protein purification. Cambridge: Academic Press; 2000. p. 271–304

21. Stofko-Hahn RE, Carr DW, Scott JD. A single step purification for recombinant proteins Characterization of a microtubule associated protein (MAP 2) fragment which associates with the type II cAMP‐dependent protein kinase. FEBS letters. 1992 May 18;302(3):274–8. doi: 10.1016/0014-5793(92)80458-s 1318232

22. Porath J, Carlsson JA, Olsson I, Belfrage G. Metal chelate affinity chromatography, a new approach to protein fractionation. Nature. 1975 Dec;258(5536):598. doi: 10.1038/258598a0 1678

23. Hochuli E, Döbeli H, Schacher A. New metal chelate adsorbent selective for proteins and peptides containing neighbouring histidine residues. Journal of Chromatography A. 1987 Jan 1;411:177–84.

24. Hochuli E, Bannwarth W, Döbeli H, Gentz R, Stüber D. Genetic approach to facilitate purification of recombinant proteins with a novel metal chelate adsorbent. Bio/technology. 1988 Nov;6(11):1321.

25. Chaga G, Hopp J, Nelson P. Immobilized metal ion affinity chromatography on Co2+‐carboxymethylaspartate–agarose Superflow, as demonstrated by one‐step purification of lactate dehydrogenase from chicken breast muscle. Biotechnology and applied biochemistry. 1999 Feb 1;29(1):19–24.

26. Chaga G, Bochkariov DE, Jokhadze GG, Hopp J, Nelson P. Natural poly-histidine affinity tag for purification of recombinant proteins on cobalt (II)-carboxymethylaspartate crosslinked agarose. Journal of Chromatography A. 1999 Dec 24;864(2):247–56. doi: 10.1016/s0021-9673(99)01008-0 10669292

27. Stubenrauch K, Bachmann A, Rudolph R, Lilie H. Purification of a viral coat protein by an engineered polyionic sequence. Journal of Chromatography B: Biomedical Sciences and Applications. 2000 Jan 14;737(1–2):77–84. doi: 10.1016/s0378-4347(99)00392-8 10681044

28. Richter SA, Stubenrauch K, Lilie H, Rudolph R. Polyionic fusion peptides function as specific dimerization motifs. Protein engineering. 2001 Oct 1;14(10):775–83. doi: 10.1093/protein/14.10.775 11739896

29. Vandemoortele G, Eyckerman S, Gevaert K. Pick a Tag and Explore the Functions of Your Pet Protein. Trends in biotechnology. 2019 Apr 27. https://doi.org/10.1016/j.tibtech.2019.03.016.

30. Cronan JE. Biotination of proteins in vivo. A post-translational modification to label, purify, and study proteins. Journal of Biological Chemistry. 1990 Jun 25;265(18):10327–33. 2113052

31. Fall RR. Analysis of microbial biotin proteins. In: McCormick D, Wright L, editors. Methods in enzymology, Volume 62. Vitamins and coenzymes, Part D. Cambridge: Academic Press; 1979. p. 390–398.

32. Fall RR, Vagelos PR. Biotin carboxyl carrier protein from Escherichia coli. In: Lowenstein J, editor. Methods in enzymology, Volume 35. Lipids, Part B. Cambridge: Academic Press; 1975. p. 17–25.

33. Fall RR, Vagelos PR. Acetyl coenzyme A carboxylase molecular forms and subunit composition of biotin carboxyl carrier protein. Journal of Biological Chemistry. 1972 Dec 25;247(24):8005–15. 4565671

34. Chapman-Smith A, Cronan JE Jr. Molecular biology of biotin attachment to proteins. The Journal of nutrition. 1999 Feb 1;129(2):477S–84S.

35. Beckett D, Kovaleva E, Schatz PJ. A minimal peptide substrate in biotin holoenzyme synthetase-catalyzed biotinylation. Protein Science. 1999 Apr;8(4):921–9. doi: 10.1110/ps.8.4.921 10211839

36. Samols D, Thornton CG, Murtif VL, Kumar GK, Haase FC, Wood HG. Evolutionary conservation among biotin enzymes. Journal of Biological Chemistry. 1988 May 15;263(14):6461–4. 2896195

37. Green NM. Avidin. In: Anfinsen CB, Edsall J, Richards F, editors. Advances in protein chemistry, Volume 29. Cambridge: Academic Press; 1975. p. 85–133. 237414

38. Laitinen OH, Hytönen VP, Nordlund HR, Kulomaa MS. Genetically engineered avidins and streptavidins. Cellular and Molecular Life Sciences CMLS. 2006 Dec 1;63(24):2992–3017. doi: 10.1007/s00018-006-6288-z 17086379

39. de Boer E, Rodriguez P, Bonte E, Krijgsveld J, Katsantoni E, Heck A, et al. Efficient biotinylation and single-step purification of tagged transcription factors in mammalian cells and transgenic mice. Proceedings of the National Academy of Sciences. 2003 Jun 24;100(13):7480–5.

40. Tenzer S, Moro A, Kuharev J, Francis AC, Vidalino L, Provenzani A et al. Proteome-wide characterization of the RNA-binding protein RALY-interactome using the in vivo-biotinylation-pulldown-quant (iBioPQ) approach. Journal of proteome research. 2013 May 6;12(6):2869–84. doi: 10.1021/pr400193j 23614458

41. Weinmann AS, Bartley SM, Zhang T, Zhang MQ, Farnham PJ. Use of chromatin immunoprecipitation to clone novel E2F target promoters. Molecular and cellular biology. 2001 Oct 15;21(20):6820–32. doi: 10.1128/MCB.21.20.6820-6832.2001 11564866

42. Weinmann AS, Farnham PJ. Identification of unknown target genes of human transcription factors using chromatin immunoprecipitation. Methods. 2002 Jan 2;26(1):37–47. doi: 10.1016/S1046-2023(02)00006-3 12054903

43. Spencer VA, Sun JM, Li L, Davie JR. Chromatin immunoprecipitation: a tool for studying histone acetylation and transcription factor binding. Methods. 2003 Sep 1;31(1):67–75. 12893175

44. Viens A, Mechold U, Lehrmann H, Harel-Bellan A, Ogryzko V. Use of protein biotinylation in vivo for chromatin immunoprecipitation. Anal Biochem. 2004 Feb 1;325(1): 68–76. doi: 10.1016/j.ab.2003.10.015 14715286

45. van Werven FJ, Timmers HT. The use of biotin tagging in Saccharomyces cerevisiae improves the sensitivity of chromatin immunoprecipitation. Nucleic acids research. 2006 Jan 1;34(4):e33–e33. doi: 10.1093/nar/gkl003 16500888

46. Kim J, Chu J, Shen X, Wang J, Orkin SH. An extended transcriptional network for pluripotency of embryonic stem cells. Cell. 2008 Mar 21;132(6):1049–61. doi: 10.1016/j.cell.2008.02.039 18358816

47. Chen I, Howarth M, Lin W, Ting AY. Site-specific labeling of cell surface proteins with biophysical probes using biotin ligase. Nat Methods. 2005 Feb 2;2(2): 99–104. doi: 10.1038/nmeth735 15782206

48. Howarth M, Takao K, Hayashi Y, Ting AY. Targeting quantum dots to surface proteins in living cells with biotin ligase. Proceedings of the National Academy of Sciences. 2005 May 24;102(21):7583–8.

49. Roux KJ, Kim DI, Raida M, Burke B. A promiscuous biotin ligase fusion protein identifies proximal and interacting proteins in mammalian cells. J Cell Biol. 2012 Mar 19;196(6):801–10. doi: 10.1083/jcb.201112098 22412018

50. Kim DI, Jensen SC, Noble KA, Birendra KC, Roux KH, Motamedchaboki K, et al. An improved smaller biotin ligase for BioID proximity labeling. Molecular biology of the cell. 2016 Apr 15;27(8):1188–96. doi: 10.1091/mbc.E15-12-0844 26912792

51. Branon TC, Bosch JA, Sanchez AD, Udeshi ND, Svinkina T, Carr SA, et al. Efficient proximity labeling in living cells and organisms with TurboID. Nature biotechnology. 2018 Sep;36(9):880. doi: 10.1038/nbt.4201 30125270

52. Fakhouri M, Elalayli M, Sherling D, Hall JD, Miller E, Sun X, et al. Minor proteins and enzymes of the Drosophila eggshell matrix. Developmental biology. 2006 May 1;293(1):127–41. doi: 10.1016/j.ydbio.2006.01.028 16515779

53. Wu T, Manogaran AL, Beauchamp JM, Waring GL. Drosophila vitelline membrane assembly: a critical role for an evolutionarily conserved cysteine in the “VM domain” of sV23. Developmental biology. 2010 Nov 15;347(2):360–8. doi: 10.1016/j.ydbio.2010.08.037 20832396

54. Jin Y, Anderson KV. Dominant and recessive alleles of the Drosophila easter gene are point mutations at conserved sites in the serine protease catalytic domain. Cell. 1990 Mar 9;60(5): 873–81. doi: 10.1016/0092-8674(90)90100-s 2107028

55. Chasan R, Jin YI, Anderson KV. Activation of the easter zymogen is regulated by five other genes to define dorsal-ventral polarity in the Drosophila embryo. Development. 1992 Jun 1;115(2): 607–16. 1425342

56. Smith CL, DeLotto R. Ventralizing signal determined by protease activation in Drosophila embryogenesis. Nature. 1994 Apr;368(6471):548. doi: 10.1038/368548a0 8139688

57. Casali A, Casanova J. The spatial control of Torso RTK activation: a C-terminal fragment of the Trunk protein acts as a signal for Torso receptor in the Drosophila embryo. Development. 2001 May 1;128(9):1709–15. 11290307

58. Sen J, Goltz JS, Konsolaki M, Schupbach T, Stein D. Windbeutel is required for function and correct subcellular localization of the Drosophila patterning protein Pipe. Development. 2000 Dec 15;127(24):5541–50. 11076773

59. Abrams EW, Cheng YL, Andrew DJ. Drosophila KDEL receptor function in the embryonic salivary gland and epidermis. PloS one. 2013 Oct 18;8(10):e77618. doi: 10.1371/journal.pone.0077618 24204897

60. Brand AH, Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development. 1993 Jun 1;118(2):401–15. 8223268

61. Rørth P. Gal4 in the Drosophila female germline. Mechanisms of development. 1998 Nov 1;78(1–2):113–8. doi: 10.1016/s0925-4773(98)00157-9 9858703

62. Queenan AM, Ghabrial A, Schupbach T. Ectopic activation of torpedo/Egfr, a Drosophila receptor tyrosine kinase, dorsalizes both the eggshell and the embryo. Development. 1997 Oct 1;124(19):3871–80. 9367443

63. Bobinnec Y, Marcaillou C, Morin X, Debec A. Dynamics of the endoplasmic reticulum during early development of Drosophila melanogaster. Cell motility and the cytoskeleton. 2003 Mar;54(3):217–25. doi: 10.1002/cm.10094 12589680

64. Stevens LM, Frohnhöfer HG, Klingler M, Nüsslein-Volhard C. Localized requirement for torso-like expression in follicle cells for development of terminal anlagen of the Drosophila embryo. Nature. 1990 Aug;346(6285):660. doi: 10.1038/346660a0 2385293

65. Martin JR, Raibaud A, Ollo R. Terminal pattern elements in Drosophila embryo induced by the torso-like protein. Nature. 1994 Feb;367(6465):741. doi: 10.1038/367741a0 8107870

66. Savant-Bhonsale S, Montell DJ. torso-like encodes the localized determinant of Drosophila terminal pattern formation. Genes & development. 1993 Dec 1;7(12b):2548–55.

67. Konrad KD, Goralski TJ, Mahowald AP. Developmental analysis of fs (1) gastrulation defective, a dorsal-group gene of Drosophila melanogaster. Roux's archives of developmental biology. 1988 Mar 1;197(2):75–91. doi: 10.1007/BF00375930 28305599

68. Konrad KD, Goralski TJ, Mahowald AP. Developmental genetics of the gastrulation defective locus in Drosophila melanogaster. Developmental biology. 1988 May 1;127(1):133–42. doi: 10.1016/0012-1606(88)90195-9 3129326

69. Konrad KD, Goralski TJ, Mahowald AP, Marsh JL. The gastrulation defective gene of Drosophila melanogaster is a member of the serine protease superfamily. Proceedings of the National Academy of Sciences. 1998 Jun 9;95(12):6819–24.

70. Stevens LM, Beuchle D, Jurcsak J, Tong X, Stein D. The Drosophila embryonic patterning determinant torsolike is a component of the eggshell. Current biology. 2003 Jun 17;13(12):1058– doi: 10.1016/s0960-9822(03)00379-8 12814553

71. Mineo A, Furriols M, Casanova J. Accumulation of the Drosophila Torso-like protein at the blastoderm plasma membrane suggests that it translocates from the eggshell. Development. 2015 Apr 1;142(7):1299–304. doi: 10.1242/dev.117630 25758463

72. Klingler M, Erdélyi M, Szabad J, Nüsslein-Volhard C. Function of torso in determining the terminal anlagen of the Drosophila embryo. Nature. 1988 Sep;335(6187):275. doi: 10.1038/335275a0 3412488

73. Sprenger F, Stevens LM, Nüsslein-Volhard C. The Drosophila gene torso encodes a putative receptor tyrosine kinase. Nature. 1989 Apr;338(6215):478. doi: 10.1038/338478a0 2927509

74. Casanova J, Struhl G. Localized surface activity of torso, a receptor tyrosine kinase, specifies terminal body pattern in Drosophila. Genes & development. 1989 Dec 1;3(12b):2025–38.

75. Henstridge MA, Johnson TK, Warr CG, Whisstock JC. Trunk cleavage is essential for Drosophila terminal patterning and can occur independently of Torso-like. Nature communications. 2014 Mar 3;5:3419. doi: 10.1038/ncomms4419 24584029

76. Cho YS, Stevens LM, Sieverman KJ, Nguyen J, Stein D. A ventrally localized protease in the Drosophila egg controls embryo dorsoventral polarity. Current Biology. 2012 Jun 5;22(11):1013–8. doi: 10.1016/j.cub.2012.03.065 22578419

77. Stein D, Cho YS, Stevens LM. Localized serine protease activity and the establishment of Drosophila embryonic dorsoventral polarity. Fly. 2013 Jul 21;7(3):161–7. doi: 10.4161/fly.25141 24047959

78. LeMosy EK, Tan YQ, Hashimoto C. Activation of a protease cascade involved in patterning the Drosophila embryo. Proceedings of the National Academy of Sciences. 2001 Apr 24;98(9):5055–60.

79. Dissing M, Giordano H, DeLotto R. Autoproteolysis and feedback in a protease cascade directing Drosophila dorsal–ventral cell fate. The EMBO journal. 2001 May 15;20(10):2387–93. doi: 10.1093/emboj/20.10.2387 11350927

80. Cho YS, Stevens LM, Stein D. Pipe-dependent ventral processing of Easter by Snake is the defining step in Drosophila embryo DV axis formation. Current Biology. 2010 Jun 22;20(12):1133–7. doi: 10.1016/j.cub.2010.04.056 20605458

81. Stein D, Roth S, Vogelsang E, Nüsslein-Volhard C. The polarity of the dorsoventral axis in the Drosophila embryo is defined by an extracellular signal. Cell. 1991 May 31;65(5):725–35. doi: 10.1016/0092-8674(91)90381-8 1904007

82. Morisato D, Anderson KV. The spätzle gene encodes a component of the extracellular signaling pathway establishing the dorsal-ventral pattern of the Drosophila embryo. Cell. 1994 Feb 25;76(4):677–88. doi: 10.1016/0092-8674(94)90507-x 8124709

83. Schneider DS, Jin Y, Morisato D, Anderson KV. A processed form of the Spatzle protein defines dorsal-ventral polarity in the Drosophila embryo. Development. 1994 May 1;120(5):1243–50. 8026333

84. Hashimoto C, Hudson KL, Anderson KV. The Toll gene of Drosophila, required for dorsal-ventral embryonic polarity, appears to encode a transmembrane protein. Cell. 1988 Jan 29;52(2):269–79. doi: 10.1016/0092-8674(88)90516-8 2449285

85. Semenza JC, Hardwick KG, Dean N, Pelham HR. ERD2, a yeast gene required for the receptor-mediated retrieval of luminal ER proteins from the secretory pathway. Cell. 1990 Jun 29;61(7):1349–57. doi: 10.1016/0092-8674(90)90698-e 2194670

86. Lewis MJ, Pelham HR. A human homologue of the yeast HDEL receptor. Nature. 1990 Nov;348(6297):162. doi: 10.1038/348162a0 2172835

87. Konsolaki M, Schüpbach T. windbeutel, a gene required for dorsoventral patterning in Drosophila, encodes a protein that has homologies to vertebrate proteins of the endoplasmic reticulum. Genes & development. 1998 Jan 1;12(1):120–31.

88. Luschnig S, Moussian B, Krauss J, Desjeux I, Perkovic J, Nüsslein-Volhard C. An F1 genetic screen for maternal-effect mutations affecting embryonic pattern formation in Drosophila melanogaster. Genetics. 2004 May 1;167(1):325–42. 15166158

89. Stein D, Charatsi I, Cho YS, Zhang Z, Nguyen J, DeLotto R, et al. Localization and activation of the Drosophila protease easter require the ER-resident saposin-like protein seele. Current Biology. 2010 Nov 9;20(21):1953–8. doi: 10.1016/j.cub.2010.09.069 20970335

90. Tagwerker C, Flick K, Cui M, Guerrero C, Dou Y, Auer B, et al. A tandem affinity tag for two-step purification under fully denaturing conditions: application in ubiquitin profiling and protein complex identification combined with in vivo cross-linking. Molecular & Cellular Proteomics. 2006 Apr 1;5(4):737–48.

91. Maine GN, Li H, Zaidi IW, Basrur V, Elenitoba-Johnson KS, Burstein E. A bimolecular affinity purification method under denaturing conditions for rapid isolation of a ubiquitinated protein for mass spectrometry analysis. nature protocols. 2010 Aug;5(8):1447. doi: 10.1038/nprot.2010.109 20671728

92. Vasilescu J, Guo X, Kast J. Identification of protein‐protein interactions using in vivo cross‐linking and mass spectrometry. Proteomics. 2004 Dec;4(12):3845–54. doi: 10.1002/pmic.200400856 15540166

93. Guerrero C, Tagwerker C, Kaiser P, Huang L. An integrated mass spectrometry-based proteomic approach: quantitative analysis of tandem affinity-purified in vivo cross-linked protein complexes (QTAX) to decipher the 26 S proteasome-interacting network. Molecular & Cellular Proteomics. 2006 Feb 1;5(2):366–78.

94. Herzberg C, Weidinger LA, Dörrbecker B, Hübner S, Stülke J, Commichau FM. SPINE: a method for the rapid detection and analysis of protein–protein interactions in vivo. Proteomics. 2007 Nov;7(22):4032–5. doi: 10.1002/pmic.200700491 17994626

95. Klockenbusch C, Kast J. Optimization of formaldehyde cross-linking for protein interaction analysis of non-tagged integrin ? 1. BioMed Research International. 2010 Jun 28;2010.

96. Parrott MB, Barry MA. Metabolic biotinylation of secreted and cell surface proteins from mammalian cells. Biochemical and biophysical research communications. 2001 Mar 9;281(4):993–1000. doi: 10.1006/bbrc.2001.4437 11237761

97. Nesbeth D, Williams SL, Chan L, Brain T, Slater NK, Farzaneh F, et al. Metabolic biotinylation of lentiviral pseudotypes for scalable paramagnetic microparticle-dependent manipulation. Molecular Therapy. 2006 Apr 1;13(4):814–22. doi: 10.1016/j.ymthe.2005.09.016 16298167

98. Barat B, Wu AM. Metabolic biotinylation of recombinant antibody by biotin ligase retained in the endoplasmic reticulum. Biomolecular engineering. 2007 Sep 1;24(3):283–91. doi: 10.1016/j.bioeng.2007.02.003 17379573

99. Predonzani A, Arnoldi F, López-Requena A, Burrone OR. In vivo site-specific biotinylation of proteins within the secretory pathway using a single vector system. BMC biotechnology. 2008 Dec;8(1):41.

100. Postel A, Letzel T, Müller F, Ehricht R, Pourquier P, Dauber M, et al. In vivo biotinylated recombinant influenza A virus hemagglutinin for use in subtype-specific serodiagnostic assays. Analytical biochemistry. 2011 Apr 1;411(1):22–31. doi: 10.1016/j.ab.2010.12.022 21172299

101. Sasset L, Petris G, Cesaratto F, Burrone OR. The VCP/p97 and YOD1 proteins have different substrate-dependent activities in endoplasmic reticulum-associated degradation (ERAD). Journal of Biological Chemistry. 2015 Nov 20;290(47):28175–88. doi: 10.1074/jbc.M115.656660 26463207

102. Bertuccio CA, Wang TT, Hamilton KL, Rodriguez-Gil DJ, Condliffe SB, Devor DC. Plasma membrane insertion of KCa2. 3 (SK3) is dependent upon the SNARE proteins, syntaxin-4 and SNAP23. PloS one. 2018 May 16;13(5):e0196717. doi: 10.1371/journal.pone.0196717 29768434

103. van der Meer JM. Optical clean and permanent whole mount preparations for phase-contrast microscopy of cuticular structures of insect larvae. Drosophila Information Service. 1977; 52:160.

104. Rubin GM, Spradling AC. Genetic transformation of Drosophila with transposable element vectors. Science. 1982 Oct 22;218(4570):348–53. doi: 10.1126/science.6289436 6289436

105. Coppey M, Boettiger AN, Berezhkovskii AM, Shvartsman SY. Nuclear trapping shapes the terminal gradient in the Drosophila embryo. Current Biology. 2008 Jun 24;18(12):915–9. doi: 10.1016/j.cub.2008.05.034 18571412

106. Hung V, Udeshi ND, Lam SS, Loh KH, Cox KJ, Pedram K, et al. Spatially resolved proteomic mapping in living cells with the engineered peroxidase APEX2. Nature protocols. 2016 Mar;11(3):456. doi: 10.1038/nprot.2016.018 26866790

107. Mayor U, Peng J. Deciphering tissue-specific ubiquitylation by mass spectrometry. In Ubiquitin Family Modifiers and the Proteasome 2012 (pp. 65–80). Humana Press.


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