The TULIP superfamily of eukaryotic lipid-binding proteins as a mediator of lipid sensing and transport

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1861, Issue 8, 2016, Pages 913-923

  Alva, Vikram ^a   Lupas, Andrei N ^a  

^a MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

Author keywords

BPI like; ERMES; Lipid exchange; SMP like; Takeout like; TULIP domain

Indexed keywords

ALLERGEN; BACTERICIDAL PERMEABILITY INCREASING PROTEIN; BACTERIUM LIPOPOLYSACCHARIDE; CHOLESTEROL ESTER TRANSFER PROTEIN; JUVENILE HORMONE; LIPID; LIPID BINDING PROTEIN; LIPOPOLYSACCHARIDE BINDING PROTEIN; PHOSPHOLIPID TRANSFER PROTEIN; SYNAPTOTAGMIN; TULIP PROTEIN; UNCLASSIFIED DRUG; ACUTE PHASE PROTEIN; ANTIMICROBIAL CATIONIC PEPTIDE; CARRIER PROTEIN; FATTY ACID BINDING PROTEIN; LIPOPOLYSACCHARIDE-BINDING PROTEIN; MEMBRANE PROTEIN; PLASMA PROTEIN;

ARTHROPOD; BETA SHEET; CELL ORGANELLE; EUKARYOTE; HORMONAL REGULATION; HYDROPHOBICITY; INFLAMMATION; INNATE IMMUNITY; INSECT; INSECT DEVELOPMENT; LIPID TRANSPORT; LIPOPHILICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; REVIEW; TARGET ORGAN; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; EUKARYOTIC CELL; GENETICS; HUMAN; LIPID METABOLISM; METABOLISM; MULTIGENE FAMILY; PHYLOGENY; PHYSIOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

ACUTE-PHASE PROTEINS; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; BIOLOGICAL TRANSPORT; BLOOD PROTEINS; CARRIER PROTEINS; CHOLESTEROL ESTER TRANSFER PROTEINS; EUKARYOTIC CELLS; FATTY ACID-BINDING PROTEINS; HUMANS; LIPID METABOLISM; MEMBRANE GLYCOPROTEINS; MODELS, MOLECULAR; MULTIGENE FAMILY; PHOSPHOLIPID TRANSFER PROTEINS; PHYLOGENY;

EID: 84956610457     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2016.01.016     Document Type: Review

References (110)

1. R.G. Sleight Intracellular lipid transport in eukaryotes Annu. Rev. Physiol. 49 1987 193 208
2. E. Fahy, S. Subramaniam, R.C. Murphy, M. Nishijima, C.R.H. Raetz, T. Shimizu, F. Spener, G. van Meer, M.J.O. Wakelam, and E.A. Dennis Update of the LIPID MAPS comprehensive classification system for lipids J. Lipid Res. 50 2009 S9 S14
3. G. van Meer, and A.I.P.M. de Kroon Lipid map of the mammalian cell J. Cell Sci. 124 2011 5 8
4. A. Shevchenko, and K. Simons Lipidomics: coming to grips with lipid diversity Nat. Rev. Mol. Cell Biol. 11 2010 593 598
5. M. Sud, E. Fahy, D. Cotter, A. Brown, E.A. Dennis, C.K. Glass, A.H. Merrill Jr.; R.C. Murphy, C.R. Raetz, D.W. Russell, and S. Subramaniam LMSD: LIPID MAPS structure database Nucleic Acids Res. 35 2007 D527 D532
6. G. van Meer, D.R. Voelker, and G.W. Feigenson Membrane lipids: where they are and how they behave Nat. Rev. Mol. Cell Biol. 9 2008 112 124
7. E. Muro, G.E. Atilla-Gokcumen, and U.S. Eggert Lipids in cell biology: how can we understand them better? Mol. Biol. Cell 25 2014 1819 1823
8. P. Fagone, and S. Jackowski Membrane phospholipid synthesis and endoplasmic reticulum function J. Lipid Res. 50 2009 S311 S316
9. C. Osman, D.R. Voelker, and T. Langer Making heads or tails of phospholipids in mitochondria J. Cell Biol. 192 2011 7 16
10. R.J. Wanders, and H.R. Waterham Biochemistry of mammalian peroxisomes revisited Annu. Rev. Biochem. 75 2006 295 332
11. A.J. Lusis, and P. Pajukanta A treasure trove for lipoprotein biology Nat. Genet. 40 2008 129 130
12. D.R. Voelker Lipid transport pathways in mammalian cells Experientia 46 1990 569 579
13. J.C. Holthuis, and A.K. Menon Lipid landscapes and pipelines in membrane homeostasis Nature 510 2014 48 57
14. S. Lev Non-vesicular lipid transport by lipid-transfer proteins and beyond Nat. Rev. Mol. Cell Biol. 11 2010 739 750
15. S. Lev Nonvesicular lipid transfer from the endoplasmic reticulum Cold Spring Harb. Perspect. Biol. 4 2012
16. W.A. Prinz Lipid trafficking sans vesicles: where, why, how? Cell 143 2010 870 874
17. G. van Meer, and H. Sprong Membrane lipids and vesicular traffic Curr. Opin. Cell Biol. 16 2004 373 378
18. D.B. Zilversmit Lipid transfer proteins: overview and applications Methods Enzymol. 98 1983 565 573
19. G. D'Angelo, M. Vicinanza, and M.A. De Matteis Lipid-transfer proteins in biosynthetic pathways Curr. Opin. Cell Biol. 20 2008 360 370
20. C. Raiborg, E.M. Wenzel, and H. Stenmark ER-endosome contact sites: molecular compositions and functions EMBO J. 34 2015 1848 1858
21. Y. Elbaz, and M. Schuldiner Staying in touch: the molecular era of organelle contact sites Trends Biochem. Sci. 36 2011 616 623
22. T. Levine, and C. Loewen Inter-organelle membrane contact sites: through a glass, darkly Curr. Opin. Cell Biol. 18 2006 371 378
23. S.C. Helle, G. Kanfer, K. Kolar, A. Lang, A.H. Michel, and B. Kornmann Organization and function of membrane contact sites Biochim. Biophys. Acta 1833 2013 2526 2541
24. M. Kawano, K. Kumagai, M. Nishijima, and K. Hanada Efficient trafficking of ceramide from the endoplasmic reticulum to the Golgi apparatus requires a VAMP-associated protein-interacting FFAT motif of CERT J. Biol. Chem. 281 2006 30279 30288
25. C.M. Schauder, X. Wu, Y. Saheki, P. Narayanaswamy, F. Torta, M.R. Wenk, P. De Camilli, and K.M. Reinisch Structure of a lipid-bound extended synaptotagmin indicates a role in lipid transfer Nature 510 2014 552 555
26. B. Kornmann, E. Currie, S.R. Collins, M. Schuldiner, J. Nunnari, J.S. Weissman, and P. Walter An ER-mitochondria tethering complex revealed by a synthetic biology screen Science 325 2009 477 481
27. A. Toulmay, and W.A. Prinz A conserved membrane-binding domain targets proteins to organelle contact sites J. Cell Sci. 125 2012 49 58
28. I. Lee, and W.J. Hong Diverse membrane-associated proteins contain a novel SMP domain FASEB J. 20 2006 202 206
29. K.O. Kopec, V. Alva, and A.N. Lupas Homology of SMP domains to the TULIP superfamily of lipid-binding proteins provides a structural basis for lipid exchange between ER and mitochondria Bioinformatics 26 2010 1927 1931
30. K.O. Kopec, V. Alva, and A.N. Lupas Bioinformatics of the TULIP domain superfamily Biochem. Soc. Trans. 39 2011 1033 1038
31. J. Soding, A. Biegert, and A.N. Lupas The HHpred interactive server for protein homology detection and structure prediction Nucleic Acids Res. 33 2005 W244 W248
32. X. Qiu, A. Mistry, M.J. Ammirati, B.A. Chrunyk, R.W. Clark, Y. Cong, J.S. Culp, D.E. Danley, T.B. Freeman, K.F. Geoghegan, M.C. Griffor, S.J. Hawrylik, C.M. Hayward, P. Hensley, L.R. Hoth, G.A. Karam, M.E. Lira, D.B. Lloyd, K.M. McGrath, K.J. Stutzman-Engwall, A.K. Subashi, T.A. Subashi, J.F. Thompson, I.K. Wang, H. Zhao, and A.P. Seddon Crystal structure of cholesteryl ester transfer protein reveals a long tunnel and four bound lipid molecules Nat. Struct. Mol. Biol. 14 2007 106 113
33. L.J. Beamer, S.F. Carroll, and D. Eisenberg Crystal structure of human BPI and two bound phospholipids at 2.4 angstrom resolution Science 276 1997 1861 1864
34. L.J. Beamer, D. Fischer, and D. Eisenberg Detecting distant relatives of mammalian LPS-binding and lipid transport proteins Protein Sci. 7 1998 1643 1646
35. C. Hamiaux, D. Stanley, D.R. Greenwood, E.N. Baker, and R.D. Newcomb Crystal structure of Epiphyas postvittana takeout 1 with bound ubiquinone supports a role as ligand carriers for takeout proteins in insects J. Biol. Chem. 284 2009 3496 3503
36. G.A. Mueller, L.L. Edwards, J.J. Aloor, M.B. Fessler, J. Glesner, A. Pomes, M.D. Chapman, R.E. London, and L.C. Pedersen The structure of the dust mite allergen Der p 7 reveals similarities to innate immune proteins J. Allergy Clin. Immunol. 125 2010 909 917 e904
37. R. Kolodziejczyk, G. Bujacz, M. Jakob, A. Ozyhar, M. Jaskolski, and M. Kochman Insect juvenile hormone binding protein shows ancestral fold present in human lipid-binding proteins J. Mol. Biol. 377 2008 870 881
38. K. Kawano, S.C. Qin, M. Lin, A.R. Tall, and X.C. Jiang Cholesteryl ester transfer protein and phospholipid transfer protein have nonoverlapping functions in vivo J. Biol. Chem. 275 2000 29477 29481
39. C.M. Schauder, X.D. Wu, Y. Saheki, P. Narayanaswamy, F. Torta, M.R. Wenk, P. De Camilli, and K.M. Reinisch Structure of a lipid-bound extended synaptotagmin indicates a role in lipid transfer Nature 510 2014 552 (+)
40. A.P. AhYoung, J.S. Jiang, J. Zhang, X.K. Dang, J.A. Loo, Z.H. Zhou, and P.F. Egea Conserved SMP domains of the ERMES complex bind phospholipids and mediate tether assembly Proc. Natl. Acad. Sci. U. S. A. 112 2015 E3179 E3188
41. A. Yazdanyar, C. Yeang, and X.C. Jiang Role of phospholipid transfer protein in high-density lipoprotein-mediated reverse cholesterol transport Curr. Atheroscler. Rep. 13 2011 242 248
42. R. McPherson, and Y. Marcel Role of cholesteryl ester transfer protein in reverse cholesterol transport Clin. Cardiol. 14 1991 I31 I34
43. A.R. Tall An overview of reverse cholesterol transport Eur. Heart J. 19 Suppl. A 1998 A31 A35
44. E. Bruckert, and B. Hansel HDL-c is a powerful lipid predictor of cardiovascular diseases Int. J. Clin. Pract. 61 2007 1905 1913
45. P.J. Barter, H.B. Brewer Jr.; M.J. Chapman, C.H. Hennekens, D.J. Rader, and A.R. Tall Cholesteryl ester transfer protein: a novel target for raising HDL and inhibiting atherosclerosis Arterioscler. Thromb. Vasc. Biol. 23 2003 160 167
46. M.L. Brown, A. Inazu, C.B. Hesler, L.B. Agellon, C. Mann, M.E. Whitlock, Y.L. Marcel, R.W. Milne, J. Koizumi, H. Mabuchi, and et al. Molecular basis of lipid transfer protein deficiency in a family with increased high-density lipoproteins Nature 342 1989 448 451
47. A. Inazu, M.L. Brown, C.B. Hesler, L.B. Agellon, J. Koizumi, K. Takata, Y. Maruhama, H. Mabuchi, and A.R. Tall Increased high-density lipoprotein levels caused by a common cholesteryl-ester transfer protein gene mutation N. Engl. J. Med. 323 1990 1234 1238
48. E.J. Niesor Different effects of compounds decreasing cholesteryl ester transfer protein activity on lipoprotein metabolism Curr. Opin. Lipidol. 22 2011 288 295
49. S. Liu, A. Mistry, J.M. Reynolds, D.B. Lloyd, M.C. Griffor, D.A. Perry, R.B. Ruggeri, R.W. Clark, and X. Qiu Crystal structures of cholesteryl ester transfer protein in complex with inhibitors J. Biol. Chem. 287 2012 37321 37329
50. M.A. Miyares Anacetrapib and dalcetrapib: two novel cholesteryl ester transfer protein inhibitors Ann. Pharmacother. 45 2011 84 94
51. P.J. Kappelle, A. van Tol, B.H. Wolffenbuttel, and R.P. Dullaart Cholesteryl ester transfer protein inhibition in cardiovascular risk management: ongoing trials will end the confusion Cardiovasc. Ther. 29 2011 e89 e99
52. The American Heritage dictionary of the English language, 3rd ed. ed.; Boston: Houghton Mifflin, c1992 (1996 [printing]).
53. T.L. Swenson, R.W. Brocia, and A.R. Tall Plasma cholesteryl ester transfer protein has binding sites for neutral lipids and phospholipids J. Biol. Chem. 263 1988 5150 5157
54. P.J. Barter, and M.E. Jones Kinetic studies of the transfer of esterified cholesterol between human plasma low and high density lipoproteins J. Lipid Res. 21 1980 238 249
55. J. Ihm, D.M. Quinn, S.J. Busch, B. Chataing, and J.A. Harmony Kinetics of plasma protein-catalyzed exchange of phosphatidylcholine and cholesteryl ester between plasma lipoproteins J. Lipid Res. 23 1982 1328 1341
56. A.R. Tall Plasma cholesteryl ester transfer protein J. Lipid Res. 34 1993 1255 1274
57. L. Zhang, F. Yan, S. Zhang, D. Lei, M.A. Charles, G. Cavigiolio, M. Oda, R.M. Krauss, K.H. Weisgraber, K.A. Rye, H.J. Pownall, X. Qiu, and G. Ren Structural basis of transfer between lipoproteins by cholesteryl ester transfer protein Nat. Chem. Biol. 8 2012 342 349
58. M. Zhang, R. Charles, H. Tong, L. Zhang, M. Patel, F. Wang, M.J. Rames, A. Ren, K.A. Rye, X. Qiu, D.G. Johns, M.A. Charles, and G. Ren HDL surface lipids mediate CETP binding as revealed by electron microscopy and molecular dynamics simulation Sci. Rep. 5 2015 8741
59. J.J. Albers, S. Vuletic, and M.C. Cheung Role of plasma phospholipid transfer protein in lipid and lipoprotein metabolism Biochim. Biophys. Acta 1821 2012 345 357
60. T. Gautier, and L. Lagrost Plasma PLTP (phospholipid-transfer protein): an emerging role in 'reverse lipopolysaccharide transport' and innate immunity Biochem. Soc. Trans. 39 2011 984 988
61. D. Masson, X.C. Jiang, L. Lagrost, and A.R. Tall The role of plasma lipid transfer proteins in lipoprotein metabolism and atherogenesis J. Lipid Res. 50 Suppl. 2009 S201 S206
62. T. Tatsuta, M. Scharwey, and T. Langer Mitochondrial lipid trafficking Trends Cell Biol. 24 2014 44 52
63. T. Klecker, S. Bockler, and B. Westermann Making connections: interorganelle contacts orchestrate mitochondrial behavior Trends Cell Biol. 24 2014 537 545
64. S.E. Horvath, H. Rampelt, S. Oeljeklaus, B. Warscheid, M. van der Laan, and N. Pfanner Role of membrane contact sites in protein import into mitochondria Protein Sci. 24 2015 277 297
65. J.E. Vance MAM (mitochondria-associated membranes) in mammalian cells: lipids and beyond Biochim. Biophys. Acta 1841 2014 595 609
66. S.E. Horvath, and G. Daum Lipids of mitochondria Prog. Lipid Res. 52 2013 590 614
67. G. van Meer, and A.I. de Kroon Lipid map of the mammalian cell J. Cell Sci. 124 2011 5 8
68. B. Kornmann, and P. Walter ERMES-mediated ER-mitochondria contacts: molecular hubs for the regulation of mitochondrial biology J. Cell Sci. 123 2010 1389 1393
69. S. Meeusen, and J. Nunnari Evidence for a two membrane-spanning autonomous mitochondrial DNA replisome J. Cell Biol. 163 2003 503 510
70. B. Kornmann, C. Osman, and P. Walter The conserved GTPase Gem1 regulates endoplasmic reticulum-mitochondria connections Proc. Natl. Acad. Sci. U. S. A. 108 2011 14151 14156
71. A.G. Manford, C.J. Stefan, H.L. Yuan, J.A. Macgurn, and S.D. Emr ER-to-plasma membrane tethering proteins regulate cell signaling and ER morphology Dev. Cell 23 2012 1129 1140
72. F. Giordano, Y. Saheki, O. Idevall-Hagren, S.F. Colombo, M. Pirruccello, I. Milosevic, E.O. Gracheva, S.N. Bagriantsev, N. Borgese, and P. De Camilli PI(4,5)P(2)-dependent and Ca(2 +)-regulated ER-PM interactions mediated by the extended synaptotagmins Cell 153 2013 1494 1509
73. C.M. Schauder, X. Wu, Y. Saheki, P. Narayanaswamy, F. Torta, M. Wenk, P. De Camilli, and K.M. Reinisch Structure of a lipid-bound extended synaptotagmin indicates a role in lipid transfer Mol. Biol. Cell 25 2014
74. R. Fernandez-Busnadiego, Y. Saheki, and P. De Camilli Three-dimensional architecture of extended synaptotagmin-mediated endoplasmic reticulum-plasma membrane contact sites Proc. Natl. Acad. Sci. U. S. A. 112 2015 E2004 E2013
75. C. Jamet-Vierny, V. Contamine, J. Boulay, D. Zickler, and M. Picard Mutations in genes encoding the mitochondrial outer membrane proteins Tom70 and Mdm10 of Podospora anserina modify the spectrum of mitochondrial DNA rearrangements associated with cellular death Mol. Cell. Biol. 17 1997 6359 6366
76. K.V. Koch, R. Suelmann, and R. Fischer Deletion of mdmB impairs mitochondrial distribution and morphology in Aspergillus nidulans Cell Motil. Cytoskeleton 55 2003 114 124
77. J.G. Wideman, N.E. Go, A. Klein, E. Redmond, S.W. Lackey, T. Tao, H. Kalbacher, D. Rapaport, W. Neupert, and F.E. Nargang Roles of the Mdm10, Tom7, Mdm12, and Mmm1 proteins in the assembly of mitochondrial outer membrane proteins in Neurospora crassa Mol. Biol. Cell 21 2010 1725 1736
78. J.G. Wideman, S.W. Lackey, M.A. Srayko, K.A. Norton, and F.E. Nargang Analysis of mutations in Neurospora crassa ERMES components reveals specific functions related to beta-barrel protein assembly and maintenance of mitochondrial morphology PLoS One 8 2013 e71837
79. A.B. Lang, A.T. John Peter, P. Walter, and B. Kornmann ER-mitochondrial junctions can be bypassed by dominant mutations in the endosomal protein Vps13 J. Cell Biol. 210 2015 883 890
80. Y. Elbaz-Alon, E. Rosenfeld-Gur, V. Shinder, A.H. Futerman, T. Geiger, and M. Schuldiner A dynamic interface between vacuoles and mitochondria in yeast Dev. Cell 30 2014 95 102
81. C. Honscher, M. Mari, K. Auffarth, M. Bohnert, J. Griffith, W. Geerts, M. van der Laan, M. Cabrera, F. Reggiori, and C. Ungermann Cellular metabolism regulates contact sites between vacuoles and mitochondria Dev. Cell 30 2014 86 94
82. T. Klecker, and B. Westermann Mitochondria are clamped to vacuoles for lipid transport Dev. Cell 30 2014 1 2
83. S. Lahiri, J.T. Chao, S. Tavassoli, A.K. Wong, V. Choudhary, B.P. Young, C.J. Loewen, and W.A. Prinz A conserved endoplasmic reticulum membrane protein complex (EMC) facilitates phospholipid transfer from the ER to mitochondria PLoS Biol. 12 2014 e1001969
84. J.G. Wideman The ubiquitous and ancient ER membrane protein complex (EMC): tether or not? F1000Res 4 2015 624
85. J.G. Wideman, R.M. Gawryluk, M.W. Gray, and J.B. Dacks The ancient and widespread nature of the ER-mitochondria encounter structure Mol. Biol. Evol. 30 2013 2044 2049
86. B.C. Krasity, J.V. Troll, J.P. Weiss, and M.J. McFall-Ngai LBP/BPI proteins and their relatives: conservation over evolution and roles in mutualism Biochem. Soc. Trans. 39 2011 1039 1044
87. J. Weiss Bactericidal/permeability-increasing protein (BPI) and lipopolysaccharide-binding protein (LBP): structure, function and regulation in host defence against Gram-negative bacteria Biochem. Soc. Trans. 31 2003 785 790
88. B. Beutler, and E.T. Rietschel Innate immune sensing and its roots: the story of endotoxin Nat. Rev. Immunol. 3 2003 169 176
89. J.K. Eckert, Y.J. Kim, J.I. Kim, K. Gurtler, D.Y. Oh, S. Sur, L. Lundvall, L. Hamann, A. van der Ploeg, P. Pickkers, E. Giamarellos-Bourboulis, A.V. Kubarenko, A.N. Weber, M. Kabesch, O. Kumpf, H.J. An, J.O. Lee, and R.R. Schumann The crystal structure of lipopolysaccharide binding protein reveals the location of a frequent mutation that impairs innate immunity Immunity 39 2013 647 660
90. J.B. Andrault, I. Gaillard, D. Giorgi, and S. Rouquier Expansion of the BPI family by duplication on human chromosome 20: characterization of the RY gene cluster in 20q11.21 encoding olfactory transporters/antimicrobial-like peptides Genomics 82 2003 172 184
91. E.E. Leclair Four BPI (bactericidal/permeability-increasing protein)-like genes expressed in the mouse nasal, oral, airway and digestive epithelia Biochem. Soc. Trans. 31 2003 801 805
92. C.D. Bingle, and C.J. Craven PLUNC: a novel family of candidate host defence proteins expressed in the upper airways and nasopharynx Hum. Mol. Genet. 11 2002 937 943
93. C.D. Bingle, L. Bingle, and C.J. Craven Distant cousins: genomic and sequence diversity within the BPI fold-containing (BPIF)/PLUNC protein family Biochem. Soc. Trans. 39 2011 961 965
94. A.L. Garland, W.G. Walton, R.D. Coakley, C.D. Tan, R.C. Gilmore, C.A. Hobbs, A. Tripathy, L.A. Clunes, S. Bencharit, M.J. Stutts, L. Betts, M.R. Redinbo, and R. Tarran Molecular basis for pH-dependent mucosal dehydration in cystic fibrosis airways Proc. Natl. Acad. Sci. U. S. A. 110 2013 15973 15978
95. S.J. Vance, R.E. McDonald, A. Cooper, B.O. Smith, and M.W. Kennedy The structure of latherin, a surfactant allergen protein from horse sweat and saliva J. R. Soc. Interface 10 2013 20130453
96. H.D. Zhou, G.Y. Li, Y.X. Yang, X.L. Li, S.R. Sheng, W.L. Zhang, and J. Zhao Intracellular co-localization of SPLUNC1 protein with nanobacteria in nasopharyngeal carcinoma epithelia HNE1 cells depended on the bactericidal permeability increasing protein domain Mol. Immunol. 43 2006 1864 1871
97. J. Baliwag, D.H. Barnes, and A. Johnston Cytokines in psoriasis Cytokine 73 2015 342 350
98. J.J. Mulero, B.J. Boyle, S. Bradley, J.M. Bright, S.T. Nelken, T.T. Ho, N.K. Mize, J.D. Childs, D.G. Ballinger, J.E. Ford, and F. Rupp Three new human members of the lipid transfer/lipopolysaccharide binding protein family (LT/LBP) Immunogenetics 54 2002 293 300
99. C. Hamiaux, L. Basten, D.R. Greenwood, E.N. Baker, and R.D. Newcomb Ligand promiscuity within the internal cavity of Epiphyas postvittana takeout 1 protein J. Struct. Biol. 182 2013 259 263
100. K.J. Kramer, L.L. Sanburg, F.J. Kezdy, and J.H. Law The juvenile hormone binding protein in the hemolymph of Manduca sexta Johannson (Lepidoptera: Sphingidae) Proc. Natl. Acad. Sci. U. S. A. 71 1974 493 497
101. L.I. Gilbert, N.A. Granger, and R.M. Roe The juvenile hormones: historical facts and speculations on future research directions Insect Biochem. Mol. Biol. 30 2000 617 644
102. R. Suzuki, Z. Fujimoto, T. Shiotsuki, W. Tsuchiya, M. Momma, A. Tase, M. Miyazawa, and T. Yamazaki Structural mechanism of JH delivery in hemolymph by JHBP of silkworm, Bombyx mori Sci. Rep. 1 2011 133
103. K.W. Tan, C. Jobichen, T.C. Ong, Y.F. Gao, Y.S. Tiong, K.N. Wong, F.T. Chew, J. Sivaraman, and Y.K. Mok Crystal structure of Der f 7, a dust mite allergen from Dermatophagoides farinae PLoS One 7 2012 e44850
104. M.I. Kidon, W.C. Chiang, W.K. Liew, T.C. Ong, Y.S. Tiong, K.N. Wong, A.C. Angus, S.T. Ong, Y.F. Gao, K. Reginald, X.Z. Bi, H.S. Shang, and F.T. Chew Mite component-specific IgE repertoire and phenotypes of allergic disease in childhood: the tropical perspective Pediatr. Allergy Immunol. 22 2011 202 210
105. N. Flinner, L. Ellenrieder, S.B. Stiller, T. Becker, E. Schleiff, and O. Mirus Mdm10 is an ancient eukaryotic porin co-occurring with the ERMES complex Biochim. Biophys. Acta 1833 2013 3314 3325
106. F. Peri, and M. Piazza Therapeutic targeting of innate immunity with Toll-like receptor 4 (TLR4) antagonists Biotechnol. Adv. 30 2012 251 260
107. S.R. Eddy Accelerated profile HMM searches PLoS Comput. Biol. 7 2011 e1002195
108. T. Frickey, and A. Lupas CLANS: a Java application for visualizing protein families based on pairwise similarity Bioinformatics 20 2004 3702 3704
109. S.F. Altschul, W. Gish, W. Miller, E.W. Myers, and D.J. Lipman Basic local alignment search tool J. Mol. Biol. 215 1990 403 410
110. Patrick Keeling, B.S. Leander, and A. Simpson Eukaryotes. Eukaryota, Organisms with nucleated cells Version 28 October 2009. http://tolweb.org/Eukaryotes/3/2009.10.28 The Tree of Life Web Project 2009 http://tolweb.org /