GM130 regulates pulmonary surfactant protein secretion in alveolar type II cells.
Alveolar type II cells
GM130
Golgi apparatus
surfactant protein
Journal
Science China. Life sciences
ISSN: 1869-1889
Titre abrégé: Sci China Life Sci
Pays: China
ID NLM: 101529880
Informations de publication
Date de publication:
01 2022
01 2022
Historique:
received:
22
09
2020
accepted:
05
01
2021
pubmed:
20
3
2021
medline:
29
3
2022
entrez:
19
3
2021
Statut:
ppublish
Résumé
Pulmonary surfactant is a lipid-protein complex secreted by alveolar type II epithelial cells and is essential for the maintenance of the delicate structure of mammalian alveoli to promote efficient gas exchange across the air-liquid barrier. The Golgi apparatus plays an important role in pulmonary surfactant modification and secretory trafficking. However, the physiological function of the Golgi apparatus in the transport of pulmonary surfactants is unclear. In the present study, deletion of GM130, which encodes for a matrix protein of the cis-Golgi cisternae, was shown to induce the disruption of the Golgi structure leading to impaired secretion of lung surfactant proteins and lipids. Specifically, the results of in vitro and in vivo analysis indicated that the loss of GM130 resulted in trapping of Sftpa in the endoplasmic reticulum, Sftpb and Sftpc accumulation in the Golgi apparatus, and an increase in the compensatory secretion of Sftpd. Moreover, global and epithelial-specific GM130 knockout in mice resulted in an enlargement of alveolar airspace and an increase in alveolar epithelial autophagy; however, surfactant repletion partially rescued the enlarged airspace defects in GM130-deficient mice. Therefore, our results demonstrate that GM130 and the mammalian Golgi apparatus play a critical role in the control of surfactant protein secretion in pulmonary epithelial cells.
Identifiants
pubmed: 33740186
doi: 10.1007/s11427-020-1875-x
pii: 10.1007/s11427-020-1875-x
doi:
Substances chimiques
Autoantigens
0
Golgin subfamily A member 2
0
Membrane Proteins
0
Pulmonary Surfactants
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
193-205Informations de copyright
© 2021. Science China Press and Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Allan, V.J., Thompson, H.M., and McNiven, M.A. (2002). Motoring around the Golgi. Nat Cell Biol 4, E236–E242.
pubmed: 12360306
Andreeva, A.V., Kutuzov, M.A., and Voyno-Yasenetskaya, T.A. (2007). Regulation of surfactant secretion in alveolar type II cells. Am J Physiol Lung Cell Mol Physiol 293, L259–L271.
pubmed: 17496061
Barinaga-Rementeria Ramirez, I., and Lowe, M. (2009). Golgins and GRASPs: holding the Golgi together. Semin Cell Dev Biol 20, 770–779.
Baschieri, F., Confalonieri, S., Bertalot, G., Di Fiore, P.P., Dietmaier, W., Leist, M., Crespo, P., Macara, I.G., and Farhan, H. (2014). Spatial control of Cdc42 signalling by a GM130-RasGRF complex regulates polarity and tumorigenesis. Nat Commun 5, 4839.
pubmed: 25208761
Baumgart, F., Ospina, O.L., Mingarro, I., Rodríguez-Crespo, I., and Pérez-Gil, J. (2010). Palmitoylation of pulmonary surfactant protein SP-C is critical for its functional cooperation with SP-B to sustain compression/expansion dynamics in cholesterol-containing surfactant films. Biophys J 99, 3234–3243.
pubmed: 21081071
pmcid: 2980709
Branchfield, K., Li, R., Lungova, V., Verheyden, J.M., McCulley, D., and Sun, X. (2016). A three-dimensional study of alveologenesis in mouse lung. Dev Biol 409, 429–441.
pubmed: 26632490
Brasch, F., Johnen, G., Winn-Brasch, A., Guttentag, S.H., Schmiedl, A., Kapp, N., Suzuki, Y., Müller, K.M., Richter, J., Hawgood, S., et al. (2004). Surfactant protein B in type II pneumocytes and intra-alveolar surfactant forms of human lungs. Am J Respir Cell Mol Biol 30, 449–458.
pubmed: 12972403
Cabré, E.J., Martínez-Calle, M., Prieto, M., Fedorov, A., Olmeda, B., Loura, L.M.S., and Pérez-Gil, J. (2018). Homo- and heterooligomerization of hydrophobic pulmonary surfactant proteins SP-B and SP-C in surfactant phospholipid membranes. J Biol Chem 293, 9399–9411.
pubmed: 29700110
pmcid: 6005437
Casals, C., and Cañadas, O. (2012). Role of lipid ordered/disordered phase coexistence in pulmonary surfactant function. Biochim Biophys Acta 1818, 2550–2562.
pubmed: 22659676
Crouch, E., and Wright, J.R. (2001). Surfactant proteins A and D and pulmonary host defense. Annu Rev Physiol 63, 521–554.
pubmed: 11181966
Curstedt, T., Jörnvall, H., Robertson, B., Bergman, T., and Berggren, P. (1987). Two hydrophobic low-molecular-mass protein fractions of pulmonary surfactant. Characterization and biophysical activity. Eur J Biochem 168, 255–262.
pubmed: 3665923
D’Angelo, G., Prencipe, L., Iodice, L., Beznoussenko, G., Savarese, M., Marra, P.F., Di Tullio, G., Martire, G., De Matteis, M.A., and Bonatti, S. (2009). GRASP65 and GRASP55 sequentially promote the transport of C-terminal valine-bearing cargos to and through the Golgi complex. J Biol Chem 284, 34849–34860.
pubmed: 19840934
pmcid: 2787347
Martínez-Alonso, E., Tomás, M., and Martínez-Menárguez, J.A. (2013). Golgi tubules: their structure, formation and role in intra-Golgi transport. Histochem Cell Biol 140, 327–339.
pubmed: 23812035
Froh, D., Gonzales, L.W., and Ballard, P.L. (1993). Secretion of surfactant protein A and phosphatidylcholine from type II cells of human fetal lung. Am J Respir Cell Mol Biol 8, 556–561.
pubmed: 8481236
Goerke, J. (1998). Pulmonary surfactant: functions and molecular composition. Biochim Biophys Acta 1408, 79–89.
pubmed: 9813251
Goss, V., Hunt, A.N., and Postle, A.D. (2013). Regulation of lung surfactant phospholipid synthesis and metabolism. Biochim Biophys Acta 1831, 448–458.
pubmed: 23200861
Griese, M., Kirmeier, H.G., Liebisch, G., Rauch, D., Stückler, F., Schmitz, G., and Zarbock, R. (2015). Surfactant lipidomics in healthy children and childhood interstitial lung disease. PLoS ONE 10, e0117985.
pubmed: 25692779
pmcid: 4333572
Guttentag, S. (2008). Posttranslational regulation of surfactant protein B expression. Semin Perinatol 32, 367–370.
pubmed: 18929160
pmcid: 2586979
Hakomori, S.I., and Handa, K. (2015). GM3 and cancer. Glycoconj J 32, 1–8.
pubmed: 25613425
Helenius, A., and Aebi, M. (2001). Intracellular functions of N-linked glycans. Science 291, 2364–2369.
pubmed: 11269317
Ikegami, M., and Jobe, A.H. (1998). Surfactant protein metabolism in vivo. Biochim Biophys Acta 1408, 218–225.
pubmed: 9813337
Joachim, J., Jefferies, H.B.J., Razi, M., Frith, D., Snijders, A.P., Chakravarty, P., Judith, D., and Tooze, S.A. (2015). Activation of ULK kinase and autophagy by GABARAP trafficking from the centrosome is regulated by WAC and GM130. Mol Cell 60, 899–913.
pubmed: 26687599
pmcid: 4691241
Johansson, J., and Curstedt, T. (1997). Molecular structures and interactions of pulmonary surfactant components. Eur J Biochem 244, 675–693.
pubmed: 9108235
Klionsky, D.J., Abdelmohsen, K., Abe, A., Abedin, M.J., Abeliovich, H., Acevedo Arozena, A., Adachi, H., Adams, C.M., Adams, P.D., Adeli, K., et al. (2016). Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy 12, 1–222.
pubmed: 26799652
pmcid: 4835977
Ladinsky, M.S., Mastronarde, D.N., McIntosh, J.R., Howell, K.E., and Staehelin, L.A. (1999). Golgi structure in three dimensions: functional insights from the normal rat kidney cell. J Cell Biol 144, 1135–1149.
pubmed: 10087259
pmcid: 2150572
Lawson, W.E., Cheng, D.S., Degryse, A.L., Tanjore, H., Polosukhin, V.V., Xu, X.C., Newcomb, D.C., Jones, B.R., Roldan, J., Lane, K.B., et al. (2011). Endoplasmic reticulum stress enhances fibrotic remodeling in the lungs. Proc Natl Acad Sci USA 108, 10562–10567.
pubmed: 21670280
pmcid: 3127925
Li, Q., Li, Y., Gu, B., Fang, L., Zhou, P., Bao, S., Huang, L., and Dai, X. (2015). Akt phosphorylates Wnt coactivator and chromatin effector Pygo2 at Serine 48 to antagonize its ubiquitin/proteasome-mediated degradation. J Biol Chem 290, 21553–21567.
pubmed: 26170450
pmcid: 4571880
Li, Q., Jiao, J., Li, H., Wan, H., Zheng, C., Cai, J., and Bao, S. (2018). Histone arginine methylation by Prmt5 is required for lung branching morphogenesis through repression of BMP signaling. J Cell Sci 131, jcs217406.
pubmed: 29950483
Liu, C., Mei, M., Li, Q., Roboti, P., Pang, Q., Ying, Z., Gao, F., Lowe, M., and Bao, S. (2017). Loss of the golgin GM130 causes Golgi disruption, Purkinje neuron loss, and ataxia in mice. Proc Natl Acad Sci USA 114, 346–351.
pubmed: 28028212
Marra, P., Salvatore, L., Mironov, A., Di Campli, A., Di Tullio, G., Trucco, A., Beznoussenko, G., Mironov, A., and De Matteis, M.A. (2007). The biogenesis of the Golgi ribbon: the roles of membrane input from the ER and of GM130. Mol Biol Cell 18, 1595–1608.
pubmed: 17314401
pmcid: 1855007
Matsumura, Y., Ban, N., Ueda, K., and Inagaki, N. (2006). Characterization and classification of ATP-binding cassette transporter ABCA3 mutants in fatal surfactant deficiency. J Biol Chem 281, 34503–34514.
pubmed: 16959783
Morrisey, E.E., and Hogan, B.L.M. (2010). Preparing for the first breath: genetic and cellular mechanisms in lung development. Dev Cell 18, 8–23.
pubmed: 20152174
pmcid: 3736813
Munro, S. (2011). The golgin coiled-coil proteins of the Golgi apparatus. Cold Spring Harbor Perspect Biol 3, a005256.
Nakamura, N., Rabouille, C., Watson, R., Nilsson, T., Hui, N., Slusarewicz, P., Kreis, T.E., and Warren, G. (1995). Characterization of a cis-Golgi Matrix Protein, GM130. J Cell Biol 131, 1715–1726.
pubmed: 8557739
Orgeig, S., Hiemstra, P.S., Veldhuizen, E.J.A., Casals, C., Clark, H.W., Haczku, A., Knudsen, L., and Possmayer, F. (2010). Recent advances in alveolar biology: evolution and function of alveolar proteins. Respir Physiol Neurobiol 173, S43–S54.
pubmed: 20433956
pmcid: 4097100
Paladino, S., Lebreton, S., Tivodar, S., Formiggini, F., Ossato, G., Gratton, E., Tramier, M., Coppey-Moisan, M., and Zurzolo, C. (2014). Golgi sorting regulates organization and activity of GPI proteins at apical membranes. Nat Chem Biol 10, 350–357.
pubmed: 24681536
pmcid: 4027978
Puthenveedu, M.A., Bachert, C., Puri, S., Lanni, F., and Linstedt, A.D. (2006). GM130 and GRASP65-dependent lateral cisternal fusion allows uniform Golgi-enzyme distribution. Nat Cell Biol 8, 238–248.
pubmed: 16489344
Qua Hiansen, J., Keating, E., Aspros, A., Yao, L.J., Bosma, K.J., Yamashita, C.M., Lewis, J.F., and Veldhuizen, R.A.W. (2015). Cholesterol-mediated surfactant dysfunction is mitigated by surfactant protein A. Biochim Biophys Acta 1848, 813–820.
Roldan, N., Goormaghtigh, E., Pérez-Gil, J., and Garcia-Alvarez, B. (2015). Palmitoylation as a key factor to modulate SP-C-lipid interactions in lung surfactant membrane multilayers. Biochim Biophys Acta 1848, 184–191.
pubmed: 25306965
Sauer, B. (1998). Inducible gene targeting in mice using the Cre/lox system. Methods 14, 381–392.
pubmed: 9608509
Serrano, A.G., and Pérez-Gil, J. (2006). Protein-lipid interactions and surface activity in the pulmonary surfactant system. Chem Phys Lipids 141, 105–118.
pubmed: 16600200
Song, J.W., Lam, S.M., Fan, X., Cao, W.J., Wang, S.Y., Tian, H., Chua, G. H., Zhang, C., Meng, F.P., Xu, Z., et al. (2020). Omics-driven systems interrogation of metabolic dysregulation in COVID-19 pathogenesis. Cell Metab 32, 188–202.e5.
pubmed: 32610096
pmcid: 7311890
ten Brinke, A., Batenburg, J.J., Gadella, B.M., Haagsman, H.P., Vaandrager, A.B., and van Golde, L.M.G. (2001). The juxtamembrane lysine and arginine residues of surfactant protein C precursor influence palmitoylation via effects on trafficking. Am J Respir Cell Mol Biol 25, 156–163.
pubmed: 11509324
ten Brinke, A., van Golde, L.M.G., and Batenburg, J.J. (2002). Palmitoylation and processing of the lipopeptide surfactant protein C. Biochim Biophys Acta 1583, 253–265.
pubmed: 12176392
Tichelaar, J.W., Lu, W., and Whitsett, J.A. (2000). Conditional expression of fibroblast growth factor-7 in the developing and mature lung. J Biol Chem 275, 11858–11864.
pubmed: 10766812
van Meer, G. (1998). Lipids of the Golgi membrane. Trends Cell Biol 8, 29–33.
pubmed: 9695805
van Meer, G., and Hoetzl, S. (2010). Sphingolipid topology and the dynamic organization and function of membrane proteins. FEBS Lett 584, 1800–1805.
pubmed: 19837070
Wang, C., Ye, M., Zhao, Q., Xia, M., Liu, D., He, L., Chen, G., Peng, Y., and Liu, H. (2019). Loss of the Golgi matrix protein 130 cause aberrant IgA1 glycosylation in IgA nephropathy. Am J Nephrol 49, 307–316.
pubmed: 30917363
Wang, D., Haviland, D.L., Burns, A.R., Zsigmond, E., and Wetsel, R.A. (2007). A pure population of lung alveolar epithelial type II cells derived from human embryonic stem cells. Proc Natl Acad Sci USA 104, 4449–4454.
pubmed: 17360544
pmcid: 1838621
Wei, J.H., Zhang, Z.C., Wynn, R.M., and Seemann, J. (2015). GM130 regulates Golgi-derived spindle assembly by activating TPX2 and capturing microtubules. Cell 162, 287–299.
pubmed: 26165940
pmcid: 4506739
Weide, T., Bayer, M., Köster, M., Siebrasse, J.P., Peters, R., and Barnekow, A. (2001). The Golgi matrix protein GM130: a specific interacting partner of the small GTPase rab1b. EMBO Rep 2, 336–341.
pubmed: 11306556
pmcid: 1083862
Whitsett, J.A., Wert, S.E., and Weaver, T.E. (2015). Diseases of pulmonary surfactant homeostasis. Annu Rev Pathol Mech Dis 10, 371–393.
Wong, M., and Munro, S. (2014). Membrane trafficking. The specificity of vesicle traffic to the Golgi is encoded in the golgin coiled-coil proteins. Science 346, 1256898.
pubmed: 25359980
pmcid: 4254398
Yeong, F.M. (2013). Multi-step down-regulation of the secretory pathway in mitosis: A fresh perspective on protein trafficking. Bioessays 35, 462–471.
pubmed: 23494566
pmcid: 3654163
Ying, Z., Mei, M., Zhang, P., Liu, C., He, H., Gao, F., and Bao, S. (2015). Histone arginine methylation by PRMT7 controls germinal center formation via regulating Bcl6 transcription. J Immunol 195, 1538–1547.
pubmed: 26179907
Yu, W., Fang, X., Ewald, A., Wong, K., Hunt, C.A., Werb, Z., Matthay, M. A., and Mostov, K. (2007). Formation of cysts by alveolar type II cells in three-dimensional culture reveals a novel mechanism for epithelial morphogenesis. Mol Biol Cell 18, 1693–1700.
pubmed: 17332496
pmcid: 1855040