View Item 

Show simple item record

Molecular mechanisms of Streptococcus pneumoniaeâ targeted autophagy via pneumolysin, Golgiâ resident Rab41, and Nedd4â 1â mediated K63â linked ubiquitination
dc.contributor.authorOgawa, Michinaga
dc.contributor.authorMatsuda, Ryuta
dc.contributor.authorTakada, Naoki
dc.contributor.authorTomokiyo, Mikado
dc.contributor.authorYamamoto, Shouji
dc.contributor.authorShizukusihi, Sayaka
dc.contributor.authorYamaji, Toshiyuki
dc.contributor.authorYoshikawa, Yuko
dc.contributor.authorYoshida, Mitsutaka
dc.contributor.authorTanida, Isei
dc.contributor.authorKoike, Masato
dc.contributor.authorMurai, Miyo
dc.contributor.authorMorita, Hidetoshi
dc.contributor.authorTakeyama, Haruko
dc.contributor.authorRyo, Akihide
dc.contributor.authorGuan, Jun‐lin
dc.contributor.authorYamamoto, Masahiro
dc.contributor.authorInoue, Jun‐ichiro
dc.contributor.authorYanagawa, Toru
dc.contributor.authorFukuda, Mitsunori
dc.contributor.authorKawabe, Hiroshi
dc.contributor.authorOhnishi, Makoto
dc.date.accessioned2018-08-13T18:48:44Z
dc.date.available2019-10-01T16:02:10Zen
dc.date.issued2018-08
dc.identifier.citationOgawa, Michinaga; Matsuda, Ryuta; Takada, Naoki; Tomokiyo, Mikado; Yamamoto, Shouji; Shizukusihi, Sayaka; Yamaji, Toshiyuki; Yoshikawa, Yuko; Yoshida, Mitsutaka; Tanida, Isei; Koike, Masato; Murai, Miyo; Morita, Hidetoshi; Takeyama, Haruko; Ryo, Akihide; Guan, Jun‐lin ; Yamamoto, Masahiro; Inoue, Jun‐ichiro ; Yanagawa, Toru; Fukuda, Mitsunori; Kawabe, Hiroshi; Ohnishi, Makoto (2018). "Molecular mechanisms of Streptococcus pneumoniaeâ targeted autophagy via pneumolysin, Golgiâ resident Rab41, and Nedd4â 1â mediated K63â linked ubiquitination." Cellular Microbiology 20(8): n/a-n/a.
dc.identifier.issn1462-5814
dc.identifier.issn1462-5822
dc.identifier.urihttps://hdl.handle.net/2027.42/145222
dc.description.abstractStreptococcus pneumoniae is the most common causative agent of communityâ acquired pneumonia and can penetrate epithelial barriers to enter the bloodstream and brain. We investigated intracellular fates of S. pneumoniae and found that the pathogen is entrapped by selective autophagy in pneumolysinâ and ubiquitinâ p62â LC3 cargoâ dependent manners. Importantly, following induction of autophagy, Rab41 was relocated from the Golgi apparatus to S. pneumoniaeâ containing autophagic vesicles (PcAV), which were only formed in the presence of Rab41â positive intact Golgi apparatuses. Moreover, subsequent localization and regulation of K48â and K63â linked polyubiquitin chains in and on PcAV were clearly distinguishable from each other. Finally, we found that E3 ligase Nedd4â 1 was recruited to PcAV and played a pivotal role in K63â linked polyubiquitin chain (K63Ub) generation on PcAV, promotion of PcAV formation, and elimination of intracellular S. pneumoniae. These findings suggest that Nedd4â 1â mediated K63Ub deposition on PcAV acts as a scaffold for PcAV biogenesis and efficient elimination of host cellâ invaded pneumococci.
dc.publisherWiley Periodicals, Inc.
dc.subject.otherpneumolysin
dc.subject.otherK48â and K63â linked polyUb chain
dc.subject.otherNedd4â 1
dc.subject.otherRab41 (Rab43)
dc.subject.otherselective autophagy
dc.subject.otherStreptococcus pneumoniae
dc.titleMolecular mechanisms of Streptococcus pneumoniaeâ targeted autophagy via pneumolysin, Golgiâ resident Rab41, and Nedd4â 1â mediated K63â linked ubiquitination
dc.typeArticleen_US
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelMolecular, Cellular and Developmental Biology
dc.subject.hlbtoplevelHealth Sciences
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/145222/1/cmi12846_am.pdf
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/145222/2/cmi12846.pdf
dc.identifier.doi10.1111/cmi.12846
dc.identifier.sourceCellular Microbiology
dc.identifier.citedreferenceNozawa, T., Aikawa, C., Goda, A., Maruyama, F., Hamada, S., & Nakagawa, I. ( 2012 ). The small GTPases Rab9A and Rab23 function at distinct steps in autophagy during Group A streptococcus infection. Cellular Microbiology, 14, 1149 â 1165.
dc.identifier.citedreferenceGradstedt, H., Iovino, F., & Bijlsma, J. J. ( 2013 ). Streptococcus pneumoniae invades endothelial host cells via multiple pathways and is killed in a lysosome dependent manner. PLoS one, 8. e65626
dc.identifier.citedreferenceGrumati, P., & Dikic, I. ( 2017 ). Ubiquitin signaling and autophagy. The Journal of Biological Chemistry, jbc.TM117.000117.
dc.identifier.citedreferenceHaas, A. K., Yoshimura, S., Stephens, D. J., Preisinger, C., Fuchs, E., & Barr, F. A. ( 2007 ). Analysis of GTPaseâ activating proteins: Rab1 and Rab43 are key Rabs required to maintain a functional Golgi complex in human cells. Journal of Cell Science, 120, 2997 â 3010.
dc.identifier.citedreferenceHaldar, A. K., Foltz, C., Finethy, R., Piro, A. S., Feeley, E. M., Pillaâ Moffett, D. M., â ¦ Coers, J. ( 2015 ). Ubiquitin systems mark pathogenâ containing vacuoles as targets for host defense by guanylate binding proteins. Proceedings of the National Academy of Sciences of the United States of America, 112, E5628 â E5637.
dc.identifier.citedreferenceHara, T., Takamura, A., Kishi, C., Iemura, S., Natsume, T., Guan, J. L., & Mizushima, N. ( 2008 ). FIP200, a ULKâ interacting protein, is required for autophagosome formation in mammalian cells. The Journal of Cell Biology, 181, 497 â 510.
dc.identifier.citedreferenceHenry, R., Shaughnessy, L., Loessner, M. J., Albertiâ Segui, C., Higgins, D. E., & Swanson, J. A. ( 2006 ). Cytolysinâ dependent delay of vacuole maturation in macrophages infected with Listeria monocytogenes. Cellular Microbiology, 8, 107 â 119.
dc.identifier.citedreferenceIchimura, Y., Waguri, S., Sou, Y. S., Kageyama, S., Hasegawa, J., Ishimura, R., â ¦ Komatsu, M. ( 2013 ). Phosphorylation of p62 activates the Keap1â Nrf2 pathway during selective autophagy. Molecular Cell, 51, 618 â 631.
dc.identifier.citedreferenceIshida, M., Ohbayashi, N., Maruta, Y., Ebata, Y., & Fukuda, M. ( 2012 ). Functional involvement of Rab1A in microtubuleâ dependent anterograde melanosome transport in melanocytes. Journal of Cell Science, 125, 5177 â 5187.
dc.identifier.citedreferenceKabeya, Y., Mizushima, N., Ueno, T., Yamamoto, A., Kirisako, T., Noda, T., â ¦ Yoshimori, T. ( 2000 ). LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. The EMBO Journal, 19, 5720 â 5728.
dc.identifier.citedreferenceKadioglu, A., Weiser, J. N., Paton, J. C., & Andrew, P. W. ( 2008 ). The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nature Reviews. Microbiology, 6, 288 â 301.
dc.identifier.citedreferenceKawabe, H., Neeb, A., Dimova, K., Young, S. M. Jr., Takeda, M., Katsurabayashi, S., et al. ( 2010 ). Regulation of Rap2A by the ubiquitin ligase Nedd4â 1 controls neurite development. Neuron, 65, 358 â 372.
dc.identifier.citedreferenceKim, J. Y., Paton, J. C., Briles, D. E., Rhee, D. K., & Pyo, S. ( 2015 ). Streptococcus pneumoniae induces pyroptosis through the regulation of autophagy in murine microglia. Oncotarget, 6, 44161 â 44178.
dc.identifier.citedreferenceKobayashi, N., Kadono, Y., Naito, A., Matsumoto, K., Yamamoto, T., Tanaka, S., & Inoue, J. ( 2001 ). Segregation of TRAF6â mediated signaling pathways clarifies its role in osteoclastogenesis. The EMBO Journal, 20, 1271 â 1280.
dc.identifier.citedreferenceKomatsu, M., Waguri, S., Koike, M., Sou, Y. S., Ueno, T., Hara, T., â ¦ Tanaka, K. ( 2007 ). Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagyâ deficient mice. Cell, 131, 1149 â 1163.
dc.identifier.citedreferenceKomatsu, M., Waguri, S., Ueno, T., Iwata, J., Murata, S., Tanida, I., â ¦ Chiba, T. ( 2005 ). Impairment of starvationâ induced and constitutive autophagy in Atg7â deficient mice. The Journal of Cell Biology, 169, 425 â 434.
dc.identifier.citedreferenceKuma, A., Hatano, M., Matsui, M., Yamamoto, A., Nakaya, H., Yoshimori, T., â ¦ Mizushima, N. ( 2004 ). The role of autophagy during the early neonatal starvation period. Nature, 432, 1032 â 1036.
dc.identifier.citedreferenceLi, P., Shi, J., He, Q., Hu, Q., Wang, Y. Y., Zhang, L. J., et al. ( 2015 ). Streptococcus pneumoniae induces autophagy through the inhibition of the PI3Kâ I/Akt/mTOR pathway and ROS hypergeneration in A549 cells. PLoS one, 10. e0122753
dc.identifier.citedreferenceLin, Q., Dai, Q., Meng, H., Sun, A., Wei, J., Peng, K., â ¦ Yang, W. ( 2017 ). The HECT E3 ubiquitin ligase NEDD4 interacts with and ubiquitinates SQSTM1 for inclusion body autophagy. Journal of Cell Science, 130, 3839 â 3850.
dc.identifier.citedreferenceLu, S. L., Kuo, C. F., Chen, H. W., Yang, Y. S., Liu, C. C., Anderson, R., et al. ( 2015 ). Insufficient acidification of autophagosomes facilitates Group A streptococcus survival and growth in endothelial cells. MBio, 6, e01435 â e01415.
dc.identifier.citedreferenceMinowaâ Nozawa, A., Nozawa, T., Okamotoâ Furuta, K., Kohda, H., & Nakagawa, I. ( 2017 ). Rab35 GTPase recruits NPD52 to autophagy targets. The EMBO Journal, 36, 2790 â 2807.
dc.identifier.citedreferenceNakagawa, I., Amano, A., Mizushima, N., Yamamoto, A., Yamaguchi, H., Kamimoto, T., â ¦ Yoshimori, T. ( 2004 ). Autophagy defends cells against invading Group A streptococcus. Science, 306, 1037 â 1040.
dc.identifier.citedreferenceNakano, S., Fujisawa, T., Ito, Y., Chang, B., Suga, S., Noguchi, T., â ¦ Ichiyama, S. ( 2016 ). Serotypes, antimicrobial susceptibility, and molecular epidemiology of invasive and nonâ invasive Streptococcus pneumoniae isolates in paediatric patients after the introduction of 13â valent conjugate vaccine in a nationwide surveillance study conducted in Japan in 2012â 2014. Vaccine, 34, 67 â 76.
dc.identifier.citedreferenceNisoâ Santano, M., Malik, S. A., Pietrocola, F., Bravoâ San Pedro, J. M., Marino, G., Cianfanelli, V., â ¦ Kroemer, G. ( 2015 ). Unsaturated fatty acids induce nonâ canonical autophagy. The EMBO Journal, 34, 1025 â 1041.
dc.identifier.citedreferenceOda, S., Nozawa, T., Nozawaâ Minowa, A., Tanaka, M., Aikawa, C., Harada, H., & Nakagawa, I. ( 2016 ). Golgiâ resident GTPase Rab30 promotes the biogenesis of pathogenâ containing autophagosomes. PLoS one, 11. e0147061
dc.identifier.citedreferenceOgawa, M., Yoshikawa, Y., Kobayashi, T., Mimuro, H., Fukumatsu, M., Kiga, K., â ¦ Sasakawa, C. ( 2011 ). A Tecpr1â dependent selective autophagy pathway targets bacterial pathogens. Cell Host & Microbe, 9, 376 â 389.
dc.identifier.citedreferenceOgawa, M., Yoshimori, T., Suzuki, T., Sagara, H., Mizushima, N., & Sasakawa, C. ( 2005 ). Escape of intracellular Shigella from autophagy. Science, 307, 727 â 731.
dc.identifier.citedreferenceOhbayashi, N., Maruta, Y., Ishida, M., & Fukuda, M. ( 2012 ). Melanoregulin regulates retrograde melanosome transport through interaction with the RILPâ p150Glued complex in melanocytes. Journal of Cell Science, 125, 1508 â 1518.
dc.identifier.citedreferencePlatta, H. W., Abrahamsen, H., Thoresen, S. B., & Stenmark, H. ( 2012 ). Nedd4â dependent lysineâ 11â linked polyubiquitination of the tumour suppressor Beclin 1. The Biochemical Journal, 441, 399 â 406.
dc.identifier.citedreferencePozzi, G., Masala, L., Iannelli, F., Manganelli, R., Havarstein, L. S., Piccoli, L., â ¦ Morrison, D. A. ( 1996 ). Competence for genetic transformation in encapsulated strains of Streptococcus pneumoniae: Two allelic variants of the peptide pheromone. Journal of Bacteriology, 178, 6087 â 6090.
dc.identifier.citedreferenceRegevâ Yochay, G., Trzcinski, K., Thompson, C. M., Lipsitch, M., & Malley, R. ( 2007 ). SpxB is a suicide gene of Streptococcus pneumoniae and confers a selective advantage in an in vivo competitive colonization model. Journal of Bacteriology, 189, 6532 â 6539.
dc.identifier.citedreferenceSaitoh, T., Fujita, N., Jang, M. H., Uematsu, S., Yang, B. G., Satoh, T., â ¦ Akira, S. ( 2008 ). Loss of the autophagy protein Atg16L1 enhances endotoxinâ induced ILâ 1beta production. Nature, 456, 264 â 268.
dc.identifier.citedreferenceSeto, S., Tsujimura, K., & Koide, Y. ( 2011 ). Rab GTPases regulating phagosome maturation are differentially recruited to mycobacterial phagosomes. Traffic, 12, 407 â 420.
dc.identifier.citedreferenceSun, A., Wei, J., Childress, C., Shaw, J. H.t., Peng, K., Shao, G., et al. ( 2017 ). The E3 ubiquitin ligase NEDD4 is an LC3â interactive protein and regulates autophagy. Autophagy, 13, 522 â 537.
dc.identifier.citedreferenceTsuboi, T., & Fukuda, M. ( 2006 ). Rab3A and Rab27A cooperatively regulate the docking step of denseâ core vesicle exocytosis in PC12 cells. Journal of Cell Science, 119, 2196 â 2203.
dc.identifier.citedreferenceVerlhac, P., Gregoire, I. P., Azocar, O., Petkova, D. S., Baguet, J., Viret, C., & Faure, M. ( 2015 ). Autophagy receptor NDP52 regulates pathogenâ containing autophagosome maturation. Cell Host & Microbe, 17, 515 â 525.
dc.identifier.citedreferenceYamaguchi, H., Nakagawa, I., Yamamoto, A., Amano, A., Noda, T., & Yoshimori, T. ( 2009 ). An initial step of GASâ containing autophagosomeâ like vacuoles formation requires Rab7. PLoS Pathogens, 5. e1000670
dc.identifier.citedreferenceYamaji, T., & Hanada, K. ( 2014 ). Establishment of HeLa cell mutants deficient in sphingolipidâ related genes using TALENs. PLoS one, 9. e88124
dc.identifier.citedreferenceYamamoto, M., Okamoto, T., Takeda, K., Sato, S., Sanjo, H., Uematsu, S., â ¦ Akira, S. ( 2006 ). Key function for the Ubc13 E2 ubiquitinâ conjugating enzyme in immune receptor signaling. Nature Immunology, 7, 962 â 970.
dc.identifier.citedreferenceYamamoto, S., Izumiya, H., Morita, M., Arakawa, E., & Watanabe, H. ( 2009 ). Application of lambda Red recombination system to Vibrio cholerae genetics: Simple methods for inactivation and modification of chromosomal genes. Gene, 438, 57 â 64.
dc.identifier.citedreferenceYoshikawa, Y., Ogawa, M., Hain, T., Yoshida, M., Fukumatsu, M., Kim, M., â ¦ Sasakawa, C. ( 2009 ). Listeria monocytogenes ActAâ mediated escape from autophagic recognition. Nature Cell Biology, 11, 1233 â 1240.
dc.identifier.citedreferenceZhang, J. R., Mostov, K. E., Lamm, M. E., Nanno, M., Shimida, S., Ohwaki, M., & Tuomanen, E. ( 2000 ). The polymeric immunoglobulin receptor translocates pneumococci across human nasopharyngeal epithelial cells. Cell, 102, 827 â 837.
dc.identifier.citedreferenceBarnett, T. C., Cole, J. N., Riveraâ Hernandez, T., Henningham, A., Paton, J. C., Nizet, V., & Walker, M. J. ( 2015 ). Streptococcal toxins: Role in pathogenesis and disease. Cellular Microbiology, 17, 1721 â 1741.
dc.identifier.citedreferenceBeauregard, K. E., Lee, K. D., Collier, R. J., & Swanson, J. A. ( 1997 ). pHâ dependent perforation of macrophage phagosomes by listeriolysin O from Listeria monocytogenes. The Journal of Experimental Medicine, 186, 1159 â 1163.
dc.identifier.citedreferenceChao, Y., Marks, L. R., Pettigrew, M. M., & Hakansson, A. P. ( 2014 ). Streptococcus pneumoniae biofilm formation and dispersion during colonization and disease. Frontiers in Cellular and Infection Microbiology, 4, 194.
dc.identifier.citedreferenceCheong, H., Lindsten, T., Wu, J., Lu, C., & Thompson, C. B. ( 2011 ). Ammoniaâ induced autophagy is independent of ULK1/ULK2 kinases. Proceedings of the National Academy of Sciences of the United States of America, 108, 11121 â 11126.
dc.identifier.citedreferenceDesantis, A., Bruno, T., Catena, V., De Nicola, F., Goeman, F., Iezzi, S., et al. ( 2015 ). Cheâ 1â induced inhibition of mTOR pathway enables stressâ induced autophagy. The EMBO Journal, 34, 1214 â 1230.
dc.identifier.citedreferenceEchlin, H., Frank, M. W., Iverson, A., Chang, T. C., Johnson, M. D., Rock, C. O., & Rosch, J. W. ( 2016 ). Pyruvate oxidase as a critical link between metabolism and capsule biosynthesis in Streptococcus pneumoniae. PLoS Pathogens, 12. e1005951
dc.identifier.citedreferenceFujita, N., Morita, E., Itoh, T., Tanaka, A., Nakaoka, M., Osada, Y., â ¦ Yoshimori, T. ( 2013 ). Recruitment of the autophagic machinery to endosomes during infection is mediated by ubiquitin. The Journal of Cell Biology, 203, 115 â 128.
dc.identifier.citedreferenceFukuda, M., Kanno, E., Ishibashi, K., & Itoh, T. ( 2008 ). Large scale screening for novel rab effectors reveals unexpected broad Rab binding specificity. Molecular & Cellular Proteomics, 7, 1031 â 1042.
dc.identifier.citedreferenceFuruta, N., Fujita, N., Noda, T., Yoshimori, T., & Amano, A. ( 2010 ). Combinational soluble Nâ ethylmaleimideâ sensitive factor attachment protein receptor proteins VAMP8 and Vti1b mediate fusion of antimicrobial and canonical autophagosomes with lysosomes. Molecular Biology of the Cell, 21, 1001 â 1010.
dc.identifier.citedreferenceGalluzzi, L., Baehrecke, E. H., Ballabio, A., Boya, P., Bravoâ San Pedro, J. M., Cecconi, F., â ¦ Kroemer, G. ( 2017 ). Molecular definitions of autophagy and related processes. The EMBO Journal, 36, 1811 â 1836.
dc.owningcollnameInterdisciplinary and Peer-Reviewed


Files in this item

Name:
cmi12846_am.pdf
Size:
7.226MB
Format:
PDF
View/Open
Name:
cmi12846.pdf
Size:
1.784MB
Format:
PDF
View/Open

Show simple item record

Remediation of Harmful Language

The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.

Accessibility

If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.