Characterization of the Niemann-Pick C pathway in alveolar type II cells and lamellar bodies of the lung

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 302, Issue 9, 2012, Pages

  Roszell, Blair R ^a   Tao, Jian Qin ^a   Yu, Kevin J ^a   Huang, Shaohui ^a,b   Bates, Sandra R ^a,b  

^a Institute for Environmental Medicine   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Cholesterol; Low density lipoprotein; Niemann Pick C1; Niemann Pick C2; Surfactant

Indexed keywords

ACID LIPASE; BINDING PROTEIN; CHOLESTEROL; FILIPIN; NIEMANN PICK C1 PROTEIN; NIEMANN PICK C2 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL ORGANELLE; CHEMICAL ANALYSIS; CONTROLLED STUDY; GLYCOSYLATION; IMMUNOCYTOCHEMISTRY; LAMELLAR BODY; LUNG ALVEOLUS CELL; LUNG ALVEOLUS CELL TYPE 2; LUNG ALVEOLUS MACROPHAGE; MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; RAT;

ANDROSTENES; ANIMALS; ANTICHOLESTEREMIC AGENTS; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CATHEPSIN D; CELLS, CULTURED; CHOLESTEROL; CYTOPLASMIC VESICLES; GENE EXPRESSION; GLYCOPROTEINS; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; PNEUMOCYTES; PROTEIN TRANSPORT; PULMONARY ALVEOLI; RATS; RATS, SPRAGUE-DAWLEY; STEROL ESTERASE;

EID: 84860503878     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00383.2011     Document Type: Article

References (66)

1. Bartlett GR. Phosphorus assay in column chromatography. J Biol Chem 234: 466-468, 1959.
2. Bates SR, Gonzales LW, Tao JQ, Rueckert P, Ballard PL, Fisher AB. Recovery of rat type II cell surfactant components during primary cell culture. Am J Physiol Lung Cell Mol Physiol 282: L267-L276, 2002.
3. Berger AC, Salazar G, Styers ML, Newell-Litwa KA, Werner E, Maue RA, Corbett AH, Faundez V. The subcellular localization of the Niemann-Pick type C proteins depends on the adaptor complex AP-3. J Cell Sci 120: 3640-3652, 2007.
4. Bortnick AE, Favari E, Tao JQ, Francone OL, Reilly M, Zhang Y, Rothblat GH, Bates SR. Identification and characterization of rodent ABCA1 in isolated type II pneumocytes. Am J Physiol Lung Cell Mol Physiol 285: L869-L878, 2003.
5. Brasch F, Ten Brinke A, Johnen G, Ochs M, Kapp N, Muller KM, Beers MF, Fehrenbach H, Richter J, Batenburg JJ, Buhling F. Involvement of cathepsin H in the processing of the hydrophobic surfactantassociated protein C in type II pneumocytes. Am J Respir Cell Mol Biol 26: 659-670, 2002.
6. Carstea ED, Morris JA, Coleman KG, Loftus SK, Zhang D, Cummings C, Gu J, Rosenfeld MA, Pavan WJ, Krizman DB, Nagle J, Polymeropoulos MH, Sturley SL, Ioannou YA, Higgins ME, Comly M, Cooney A, Brown A, Kaneski CR, Blanchette-Mackie EJ, Dwyer NK, Neufeld EB, Chang TY, Liscum L, Strauss JF 3rd, Ohno K, Zeigler M, Carmi R, Sokol J, Markie D, O'Neill RR, van Diggelen OP, Elleder M, Patterson MC, Brady RO, Vanier MT, Pentchev PG, Tagle DA. Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science 277: 228-231, 1997.
7. Cenedella RJ. Cholesterol synthesis inhibitor U18666A and the role of sterol metabolism and trafficking in numerous pathophysiological processes. Lipids 44: 477-487, 2009.
8. Chander A, Johnson RG, Reicherter J, Fisher AB. Lung lamellar bodies maintain an acidic internal pH. J Biol Chem 261: 6126-6131, 1986.
9. Chen R, Jiang X, Sun D, Han G, Wang F, Ye M, Wang L, Zou H. Glycoproteomics analysis of human liver tissue by combination of multiple enzyme digestion and hydrazide chemistry. J Proteome Res 8: 651-661, 2009.
10. Chinoy MR, Dodia C, Fisher AB. Increased surfactant internalization by rat type II cells cultured on microporous membranes. Am J Physiol Lung Cell Mol Physiol 264: L300-L307, 1993.
11. Davidson KG, Bersten AD, Barr HA, Dowling KD, Nicholas TE, Doyle IR. Lung function, permeability, and surfactant composition in oleic acid-induced acute lung injury in rats. Am J Physiol Lung Cell Mol Physiol 279: L1091-L1102, 2000.
12. Davies JP, Chen FW, Ioannou YA. Transmembrane molecular pump activity of Niemann-Pick C1 protein. Science 290: 2295-2298, 2000.
13. Devlin C, Pipalia NH, Liao X, Schuchman EH, Maxfield FR, Tabas I. Improvement in lipid and protein trafficking in Niemann-Pick C1 cells by correction of a secondary enzyme defect. Traffic 11: 601-615, 2010.
14. DiAugustine RP. Lung concentric laminar organelle. Hydrolase activity and compositional analysis. J Biol Chem 249: 584-593, 1974.
15. Dobbs LG. Isolation and culture of alveolar type II cells. Am J Physiol Lung Cell Mol Physiol 258: L134-L147, 1990.
16. Dobbs LG, Gonzalez R, Williams MC. An improved method for isolating type II cells in high yield and purity. Am Rev Respir Dis 134: 141-145, 1986.
17. Du XM, Kumar J, Ferguson C, Schulz TA, Ong YS, Hong WJ, Prinz WA, Parton RG, Brown AJ, Yang HY. A role for oxysterol-binding protein-related protein 5 in endosomal cholesterol trafficking. J Cell Biol 192: 121-135, 2011.
18. Duck-Chong CG. The isolation of lamellar bodies and their membranous content from rat lung, lamb tracheal fluid and human amniotic fluid. Life Sci 22: 2025-2030, 1978.
19. Elleder M, Houstkova H, Zeman J, Ledvinova J, Poupetova H. Pulmonary storage with emphysema as a sign of Niemann-Pick type C2 disease (second complementation group). Report of a case. Virchows Arch 439: 206-211, 2001.
20. Fisher AB (Editor). Lung Surfactant Clearance and Cellular Processing. Austin, TX: Landes Bioscience, 1998, p. 165-189.
21. Fisher AB, Dodia C, Ruckert P, Tao JQ, Bates SR. Pathway to lamellar bodies for surfactant protein A. Am J Physiol Lung Cell Mol Physiol 299: L51-L58, 2010.
22. Garver WS, Somers K, Krishnan K, Mitchell T, Heidenreich RA, Thrall MA. The Niemann-Pick C1 protein in feline fibroblasts. Mol Genet Metab 76: 31-36, 2002.
23. Goldstein JL, Dana SE, Faust JR, Beaudet AL, Brown MS. Role of lysosomal acid lipase in metabolism of plasma low-density lipoprotein: observations in cultured fibroblasts from a patient with cholesteryl ester storage disease. J Biol Chem 250: 8487-8495, 1975.
24. Griese M, Brasch F, Aldana VR, Cabrera MM, Goelnitz U, Ikonen E, Karam BJ, Liebisch G, Linder MD, Lohse P, Meyer W, Schmitz G, Pamir A, Ripper J, Rolfs A, Schams A, Lezana FJ. Respiratory disease in Niemann-Pick type C2 is caused by pulmonary alveolar proteinosis. Clin Genet 77: 119-130, 2010.
25. Hass MA, Longmore WJ. Surfactant cholesterol metabolism of the isolated perfused rat lung. Biochim Biophys Acta 573: 166-174, 1979.
26. Hook GE, Gilmore LB. Hydrolases of pulmonary lysosomes and lamellar bodies. J Biol Chem 257: 9211-9220, 1982.
27. Ikonen E, Baumann M, Gron K, Syvanen AC, Enomaa N, Halila R, Aula P, Peltonen L. Aspartylglucosaminuria: cDNA encoding human aspartylglucosaminidase and the missense mutation causing the disease. EMBO J 10: 51-58, 1991.
28. Infante RE, Radhakrishnan A, Abi-Mosleh L, Kinch LN, Wang ML, Grishin NV, Goldstein JL, Brown MS. Purified NPC1 protein. II. Localization of sterol binding to a 240-amino acid soluble luminal loop. J Biol Chem 283: 1064-1075, 2008.
29. Ioannou YA. Guilty until proven innocent: the case of NPC1 and cholesterol. Trends Biochem Sci 30: 498-505, 2005.
30. Johnson WJ, Phillips MC, Rothblat GH. Lipoproteins and cellular cholesterol homeostasis. Subcell Biochem 28: 235-276, 1997.
31. Kazi AS, Tao JQ, Feinstein SI, Zhang L, Fisher AB, Bates SR. Role of the PI3-kinase signaling pathway in trafficking of the surfactant protein A receptor P63 (CKAP4) on type II pneumocytes. Am J Physiol Lung Cell Mol Physiol 299: L794-L807, 2010.
32. Ko DC, Gordon MD, Jin JY, Scott MP. Dynamic movements of organelles containing Niemann-Pick C1 protein: NPC1 involvement in late endocytic events. Mol Biol Cell 12: 601-614, 2001.
33. Kwon HJ, Abi-Mosleh L, Wang ML, Deisenhofer J, Goldstein JL, Brown MS, Infante RE. Structure of N-terminal domain of NPC1 reveals distinct subdomains for binding and transfer of cholesterol. Cell 137: 1213-1224, 2009.
34. Lajoie P, Guay G, Dennis JW, Nabi IR. The lipid composition of autophagic vacuoles regulates expression of multilamellar bodies. J Cell Sci 118: 1991-2003, 2005.
35. Lange Y, Ye J, Rigney M, Steck T. Cholesterol movement in Niemann- Pick type C cells and in cells treated with amphiphiles. J Biol Chem 275: 17468-17475, 2000.
36. Lewis JA, Rao KM, Castranova V, Vallyathan V, Dennis WE, Knechtges PL. Proteomic analysis of bronchoalveolar lavage fluid: effect of acute exposure to diesel exhaust particles in rats. Environ Health Perspect 115: 756-763, 2007.
37. Liou HL, Dixit SS, Xu S, Tint GS, Stock AM, Lobel P. NPC2, the protein deficient in Niemann-Pick C2 disease, consists of multiple glycoforms that bind a variety of sterols. J Biol Chem 281: 36710-36723, 2006.
38. Loftus SK, Morris JA, Carstea ED, Gu JZ, Cummings C, Brown A, Ellison J, Ohno K, Rosenfeld MA, Tagle DA, Pentchev PG, Pavan WJ. Murine model of Niemann-Pick C disease: mutation in a cholesterol homeostasis gene. Science 277: 232-235, 1997.
39. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275, 1951.
40. Morisot C, Millat G, Coeslier A, Bourgois B, Fontenoy E, Dobbelaere D, Verot L, Haouari N, Vaillant C, Gottrand F, Bogaert E, Thelliez P, Klosowski S, Djebara A, Bachiri A, Manouvrier S, Vanier MT. [Fatal neonatal respiratory distress in Niemann-Pick C2 and prenatal diagnosis with mutations in gene HE1/NPC2]. Arch Pediatr 12: 434-437, 2005.
41. Naureckiene S, Sleat DE, Lackland H, Fensom A, Vanier MT, Wattiaux R, Jadot M, Lobel P. Identification of HE1 as the second gene of Niemann-Pick C disease. Science 290: 2298-2301, 2000.
42. Nicholson AG, Florio R, Hansell DM, Bois RM, Wells AU, Hughes P, Ramadan HK, Mackinlay CI, Brambilla E, Ferretti GR, Erichsen A, Malone M, Lantuejoul S. Pulmonary involvement by Niemann-Pick disease. A report of six cases. Histopathology 48: 596-603, 2006.
43. Palmeri S, Tarugi P, Sicurelli F, Buccoliero R, Malandrini A, De Santi MM, Marciano G, Battisti C, Dotti MT, Calandra S, Federico A. Lung involvement in Niemann-Pick disease type C1: improvement with bronchoalveolar lavage. Neurol Sci 26: 171-173, 2005.
44. Patel SC, Suresh S, Kumar U, Hu CY, Cooney A, Blanchette-Mackie EJ, Neufeld EB, Patel RC, Brady RO, Patel YC, Pentchev PG, Ong WY. Localization of Niemann-Pick C1 protein in astrocytes: implications for neuronal degeneration in Niemann-Pick type C disease. Proc Natl Acad Sci USA 96: 1657-1662, 1999.
45. Paulusma CC, de Waart DR, Kunne C, Mok KS, Elferink RP. Activity of the bile salt export pump (ABCB11) is critically dependent on canalicular membrane cholesterol content. J Biol Chem 284: 9947-9954, 2009.
46. Peake KB, Vance JE. Defective cholesterol trafficking in Niemann-Pick C-deficient cells. FEBS Lett 584: 2731-2739, 2010.
47. Perez-Gil J, Weaver TE. Pulmonary surfactant pathophysiology: current models and open questions. Physiology (Bethesda) 25: 132-141, 2010.
48. Pipalia NH, Huang A, Ralph H, Rujoi M, Maxfield FR. Automated microscopy screening for compounds that partially revert cholesterol accumulation in Niemann-Pick C cells. J Lipid Res 47: 284-301, 2006.
49. Podechard N, Le Ferrec E, Rebillard A, Fardel O, Lecureur V. NPC1 repression contributes to lipid accumulation in human macrophages exposed to environmental aryl hydrocarbons. Cardiovasc Res 82: 361-370, 2009.
50. Ribeiro I, Marcao A, Amaral O, Sa Miranda MC, Vanier MT, Millat G. Niemann-Pick type C disease: NPC1 mutations associated with severe and mild cellular cholesterol trafficking alterations. Hum Genet 109: 24-32, 2001.
51. Ridsdale R, Na CL, Xu Y, Greis KD, Weaver T. Comparative proteomic analysis of lung lamellar bodies and lysosome-related organelles. PLos One 6: e16482, 2011.
52. Schofer O, Mischo B, Puschel W, Harzer K, Vanier MT. Early-lethal pulmonary form of Niemann-Pick type C disease belonging to a second, rare genetic complementation group. Eur J Pediatr 157: 45-49, 1998.
53. Sleat DE, Wiseman JA, El-Banna M, Price SM, Verot L, Shen MM, Tint GS, Vanier MT, Walkley SU, Lobel P. Genetic evidence for nonredundant functional cooperativity between NPC1 and NPC2 in lipid transport. Proc Natl Acad Sci USA 101: 5886-5891, 2004.
54. van Weeren L, de Graaff AM, Jamieson JD, Batenburg JJ, Valentijn JA. Rab3D and actin reveal distinct lamellar body subpopulations in alveolar epithelial type II cells. Am J Respir Cell Mol Biol 30: 288-295, 2004.
55. Veldhuizen R, Nag K, Orgeig S, Possmayer F. The role of lipids in pulmonary surfactant. Biochim Biophys Acta 1408: 90-108, 1998.
56. Wang ML, Motamed M, Infante RE, Abi-Mosleh L, Kwon HJ, Brown MS, Goldstein JL. Identification of surface residues on Niemann-Pick C2 essential for hydrophobic handoff of cholesterol to NPC1 in lysosomes. Cell Metab 12: 166-173, 2010.
57. Wang P, Chintagari NR, Narayanaperumal J, Ayalew S, Hartson S, Liu L. Proteomic analysis of lamellar bodies isolated from rat lungs. BMC Cell Biol 9: 34, 2008.
58. Warshamana GS, Corti M, Brody AR. TNF-α, PDGF, and TGF-β1 expression by primary mouse bronchiolar-alveolar epithelial and mesenchymal cells: TNF-α induces TGF-β1. Exp Mol Pathol 71: 13-33, 2001.
59. Watari H, Blanchette-Mackie EJ, Dwyer NK, Watari M, Neufeld EB, Patel S, Pentchev PG, Strauss JF 3rd. Mutations in the leucine zipper motif and sterol-sensing domain inactivate the Niemann-Pick C1 glycoprotein. J Biol Chem 274: 21861-21866, 1999.
60. Weaver TE, Na CL, Stahlman M. Biogenesis of lamellar bodies, lysosome-related organelles involved in storage and secretion of pulmonary surfactant. Semin Cell Dev Biol 13: 263-270, 2002.
61. Wu YZ, Manevich Y, Baldwin JL, Dodia C, Yu K, Feinstein SI, Fisher AB. Interaction of surfactant protein A with peroxiredoxin 6 regulates phospholipase A2 activity. J Biol Chem 281: 7515-7525, 2006.
62. Xie C, Turley SD, Dietschy JM. Cholesterol accumulation in tissues of the Niemann-pick type C mouse is determined by the rate of lipoproteincholesterol uptake through the coated-pit pathway in each organ. Proc Natl Acad Sci USA 96: 11992-11997, 1999.
63. Xu S, Benoff B, Liou HL, Lobel P, Stock AM. Structural basis of sterol binding by NPC2, a lysosomal protein deficient in Niemann-Pick type C2 disease. J Biol Chem 282: 23525-23531, 2007.
64. Yamano G, Funahashi H, Kawanami O, Zhao LX, Ban N, Uchida Y, Morohoshi T, Ogawa J, Shioda S, Inagaki N. ABCA3 is a lamellar body membrane protein in human lung alveolar type II cells. FEBS Lett 508: 221-225, 2001.
65. Zen K, Notarfrancesco K, Oorschot V, Slot JW, Fisher AB, Shuman H. Generation and characterization of monoclonal antibodies to alveolar type II cell lamellar body membrane. Am J Physiol Lung Cell Mol Physiol 275: L172-L183, 1998.
66. Zhang L, Yu KJ, Robert KW, Debolt KM, Hong N, Tao JQ, Fukuda M, Fisher AB, Huang S. Rab38 targets to lamellar bodies and normalizes their sizes in lung alveolar type II epithelial cells. Am J Physiol Lung Cell Mol Physiol 301: L471-L477, 2011.