Mechanism of Lamellar Body Formation by Lung Surfactant Protein B

Adams, 2010, PHENIX: a comprehensive Python-based system for macromolecular structure solution, Acta Crystallogr. D Biol. Crystallogr., 66, 213, 10.1107/S0907444909052925 Aggarwal, 2011, Central nervous system myelin: structure, synthesis and assembly, Trends Cell Biol., 21, 585, 10.1016/j.tcb.2011.06.004 Ahn, 2003, Crystal structure of saposin B reveals a dimeric shell for lipid binding, Proc. Natl. Acad. Sci. USA, 100, 38, 10.1073/pnas.0136947100 Aida, 2015, Cloning-free CRISPR/Cas system facilitates functional cassette knock-in in mice, Genome Biol., 16, 87, 10.1186/s13059-015-0653-x Akinbi, 1997, Rescue of SP-B knockout mice with a truncated SP-B proprotein. Function of the C-terminal propeptide, J. Biol. Chem., 272, 9640, 10.1074/jbc.272.15.9640 Beck, 2000, The role of homodimers in surfactant protein B function in vivo, J. Biol. Chem., 275, 3365, 10.1074/jbc.275.5.3365 Benson, 1984, Role of calcium ions the structure and function of pulmonary surfactant, Biochim. Biophys. Acta, 793, 18, 10.1016/0005-2760(84)90048-1 Bernhard, 2016, Lung surfactant: Function and composition in the context of development and respiratory physiology, Ann. Anat., 208, 146, 10.1016/j.aanat.2016.08.003 Bian, 2011, Structures of the atlastin GTPase provide insight into homotypic fusion of endoplasmic reticulum membranes, Proc. Natl. Acad. Sci. USA, 108, 3976, 10.1073/pnas.1101643108 Bligh, 1959, A rapid method of total lipid extraction and purification, Can. J. Biochem. Physiol., 37, 911, 10.1139/y59-099 Brasch, 2004, Surfactant protein B in type II pneumocytes and intra-alveolar surfactant forms of human lungs, Am. J. Respir. Cell Mol. Biol., 30, 449, 10.1165/rcmb.2003-0262OC Bruhn, 2005, A short guided tour through functional and structural features of saposin-like proteins, Biochem. J., 389, 249, 10.1042/BJ20050051 Chander, 1983, Isolation of lamellar bodies from rat granular pneumocytes in primary culture, Biochim. Biophys. Acta, 753, 119, 10.1016/0005-2760(83)90105-4 Chander, 1986, Lung lamellar bodies maintain an acidic internal pH, J. Biol. Chem., 261, 6126, 10.1016/S0021-9258(17)38501-0 Clark, 1995, Targeted disruption of the surfactant protein B gene disrupts surfactant homeostasis, causing respiratory failure in newborn mice, Proc. Natl. Acad. Sci. USA, 92, 7794, 10.1073/pnas.92.17.7794 Cong, 2013, Multiplex genome engineering using CRISPR/Cas systems, Science, 339, 819, 10.1126/science.1231143 Derman, 1993, Mutations that allow disulfide bond formation in the cytoplasm of Escherichia coli, Science, 262, 1744, 10.1126/science.8259521 Diemel, 2002, Effects of cholesterol on surface activity and surface topography of spread surfactant films, Biochemistry, 41, 15007, 10.1021/bi0256532 Echaide, 2017, Restoring pulmonary surfactant membranes and films at the respiratory surface, Biochim. Biophys. Acta Biomembr., 1859, 1725, 10.1016/j.bbamem.2017.03.015 Emsley, 2004, Coot: model-building tools for molecular graphics, Acta Crystallogr. D Biol. Crystallogr., 60, 2126, 10.1107/S0907444904019158 Evans, 2013, How good are my data and what is the resolution?, Acta Crystallogr. D Biol. Crystallogr., 69, 1204, 10.1107/S0907444913000061 Galietta, 2001, Green fluorescent protein-based halide indicators with improved chloride and iodide affinities, FEBS Lett., 499, 220, 10.1016/S0014-5793(01)02561-3 Gerson, 2008, Pepsinogen C proteolytic processing of surfactant protein B, J. Biol. Chem., 283, 10330, 10.1074/jbc.M707516200 Greenspan, 1993, Detection by nile red of agarose gel electrophoresed native and modified low density lipoprotein, Electrophoresis, 14, 65, 10.1002/elps.1150140111 Kabsch, 2010, Xds, Acta Crystallogr. D Biol. Crystallogr., 66, 125, 10.1107/S0907444909047337 King, 1982, Pulmonary surfactant, J. Appl. Physiol., 53, 1, 10.1152/jappl.1982.53.1.1 Kolter, 2005, Principles of lysosomal membrane digestion: stimulation of sphingolipid degradation by sphingolipid activator proteins and anionic lysosomal lipids, Annu. Rev. Cell Dev. Biol., 21, 81, 10.1146/annurev.cellbio.21.122303.120013 Korimilli, 2000, Intracellular localization of processing events in human surfactant protein B biosynthesis, J. Biol. Chem., 275, 8672, 10.1074/jbc.275.12.8672 Labun, 2019, CHOPCHOP v3: expanding the CRISPR web toolbox beyond genome editing, Nucleic Acids Res., 47, W171, 10.1093/nar/gkz365 Li, 2019, Metabolic labelling of choline phospholipids probes ABCA3 transport in lamellar bodies, Biochim. Biophys. Acta Mol. Cell Biol. Lipids, 1864, 158516, 10.1016/j.bbalip.2019.158516 Liekkinen, 2020, Pulmonary surfactant lipid reorganization induced by the adsorption of the oligomeric surfactant protein B complex, J. Mol. Biol., 432, 3251, 10.1016/j.jmb.2020.02.028 Lin, 1996, Structural requirements for targeting of surfactant protein B (SP-B) to secretory granules in vitro and in vivo, J. Biol. Chem., 271, 19689, 10.1074/jbc.271.33.19689 Lin, 1996, Structural requirements for intracellular transport of pulmonary surfactant protein B (SP-B), Biochim. Biophys. Acta, 1312, 177, 10.1016/0167-4889(95)00201-4 Lopez-Rodriguez, 2017, Lung surfactant metabolism: early in life, early in disease and target in cell therapy, Cell Tissue Res., 367, 721, 10.1007/s00441-016-2520-9 Martínez-Calle, 2020, Pulmonary surfactant protein SP-B nanorings induce the multilamellar organization of surfactant complexes, Biochim. Biophys. Acta Biomembr., 1862, 183216, 10.1016/j.bbamem.2020.183216 Mathialagan, 1990, Low-molecular-weight hydrophobic proteins from bovine pulmonary surfactant, Biochim. Biophys. Acta, 1045, 121, 10.1016/0005-2760(90)90140-S Matsumura, 2007, ABCA3-mediated choline-phospholipids uptake into intracellular vesicles in A549 cells, FEBS Lett., 581, 3139, 10.1016/j.febslet.2007.05.078 Morin, 2013, Collaboration gets the most out of software, eLife, 2, e01456, 10.7554/eLife.01456 Nogee, 1993, Brief report: deficiency of pulmonary surfactant protein B in congenital alveolar proteinosis, N. Engl. J. Med., 328, 406, 10.1056/NEJM199302113280606 Nogee, 2000, Allelic heterogeneity in hereditary surfactant protein B (SP-B) deficiency, Am. J. Respir. Crit. Care Med., 161, 973, 10.1164/ajrccm.161.3.9903153 Olmeda, 2013, Structure-function correlations of pulmonary surfactant protein SP-B and the saposin-like family of proteins, Eur. Biophys. J., 42, 209, 10.1007/s00249-012-0858-9 Olmeda, 2015, A model for the structure and mechanism of action of pulmonary surfactant protein B, FASEB J., 29, 4236, 10.1096/fj.15-273458 Olofsson, 1999, The assembly and secretion of apolipoprotein B-containing lipoproteins, Curr. Opin. Lipidol., 10, 341, 10.1097/00041433-199908000-00008 Pettersen, 2004, UCSF Chimera--a visualization system for exploratory research and analysis, J. Comput. Chem., 25, 1605, 10.1002/jcc.20084 Phillips, 2018, Is ABCA1 a lipid transfer protein?, J. Lipid Res., 59, 749, 10.1194/jlr.R082313 Popovic, 2012, Structure of saposin A lipoprotein discs, Proc. Natl. Acad. Sci. USA, 109, 2908, 10.1073/pnas.1115743109 Poulain, 1992, Effects of surfactant apolipoproteins on liposome structure: implications for tubular myelin formation, Am. J. Physiol., 262, L730 Powers, 2017, Reconstitution of the tubular endoplasmic reticulum network with purified components, Nature, 543, 257, 10.1038/nature21387 Rabouille, 2016, GRASP: A Multitasking Tether, Front. Cell Dev. Biol., 4, 1, 10.3389/fcell.2016.00001 Ridsdale, 2011, Comparative proteomic analysis of lung lamellar bodies and lysosome-related organelles, PLoS ONE, 6, e16482, 10.1371/journal.pone.0016482 Rodríguez, 2009, Crystallographic ab initio protein structure solution below atomic resolution, Nat. Methods, 6, 651, 10.1038/nmeth.1365 Schneider, 2012, NIH Image to ImageJ: 25 years of image analysis, Nat. Methods, 9, 671, 10.1038/nmeth.2089 Sirwi, 2018, Lipid transfer proteins in the assembly of apoB-containing lipoproteins, J. Lipid Res., 59, 1094, 10.1194/jlr.R083451 Smith, 1988, Mixtures of low molecular weight surfactant proteins and dipalmitoyl phosphatidylcholine duplicate effects of pulmonary surfactant in vitro and in vivo, Pediatr. Res., 23, 484, 10.1203/00006450-198805000-00010 Stahlman, 2000, Lamellar body formation in normal and surfactant protein B-deficient fetal mice, Lab. Invest., 80, 395, 10.1038/labinvest.3780044 Stratton, 1976, The three-dimensional aspect of mammalian lung multilamellar bodies, Tissue Cell, 8, 693, 10.1016/0040-8166(76)90040-9 Stratton, 1978, The ultrastructure of multilamellar bodies and surfactant in the human lung, Cell Tissue Res., 193, 219, 10.1007/BF00209036 Suzuki, 1989, Reconstitution of tubular myelin from synthetic lipids and proteins associated with pig pulmonary surfactant, Am. Rev. Respir. Dis., 140, 75, 10.1164/ajrccm/140.1.75 Tanaka, 1986, Development of synthetic lung surfactants, J. Lipid Res., 27, 475, 10.1016/S0022-2275(20)35198-1 Terwilliger, 2008, Iterative model building, structure refinement and density modification with the PHENIX AutoBuild wizard, Acta Crystallogr. D Biol. Crystallogr., 64, 61, 10.1107/S090744490705024X Ueno, 2004, Processing of pulmonary surfactant protein B by napsin and cathepsin H, J. Biol. Chem., 279, 16178, 10.1074/jbc.M312029200 Vaccaro, 1999, Saposins and their interaction with lipids, Neurochem. Res., 24, 307, 10.1023/A:1022530508763 Waterhouse, 2018, SWISS-MODEL: homology modelling of protein structures and complexes, Nucleic Acids Res., 46, W296, 10.1093/nar/gky427 Weaver, 2002, Biogenesis of lamellar bodies, lysosome-related organelles involved in storage and secretion of pulmonary surfactant, Semin. Cell Dev. Biol., 13, 263, 10.1016/S1084952102000551 Wikenheiser, 1993, Production of immortalized distal respiratory epithelial cell lines from surfactant protein C/simian virus 40 large tumor antigen transgenic mice, Proc. Natl. Acad. Sci. USA, 90, 11029, 10.1073/pnas.90.23.11029 Wilkins, 1999, Protein identification and analysis tools in the ExPASy server, Methods Mol. Biol., 112, 531 Williams, 1991, Changes in lipid structure produced by surfactant proteins SP-A, SP-B, and SP-C, Am. J. Respir. Cell Mol. Biol., 5, 41, 10.1165/ajrcmb/5.1.41 Wong, 2019, Lipid transfer proteins: the lipid commute via shuttles, bridges and tubes, Nat. Rev. Mol. Cell Biol., 20, 85, 10.1038/s41580-018-0071-5 Wu, 2020, Risk factors associated with acute respiratory distress syndrome and death in patients with coronavirus disease 2019 pneumonia in Wuhan, China, JAMA Intern. Med., 180, 934, 10.1001/jamainternmed.2020.0994 Xu, 2018, CavityPlus: a web server for protein cavity detection with pharmacophore modelling, allosteric site identification and covalent ligand binding ability prediction, Nucleic Acids Res., 46, W374, 10.1093/nar/gky380 Yang, 2010, Surfactant protein B propeptide contains a saposin-like protein domain with antimicrobial activity at low pH, J. Immunol., 184, 975, 10.4049/jimmunol.0900650 Zheng, 2017, CheckMyMetal: a macromolecular metal-binding validation tool, Acta Crystallogr. D Struct. Biol., 73, 223, 10.1107/S2059798317001061