Subversion of RAB5-regulated autophagy by the intracellular pathogen Ehrlichia chaffeensis

Small GTPases

Volumn 10, Issue 5, 2019, Pages 343-349

  Rikihisa, Yasuko ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

autophagy; BECN1; class III PtdIns3K; Ehrlichia chaffeensis; endosome; Etf 1; infection; obligatory intracellular; RAB5; type IV secretion

Indexed keywords

BECLIN 1; DOXYCYCLINE; PHOSPHATIDYLINOSITOL 3 KINASE; RAB PROTEIN; SERINE THREONINE PROTEIN KINASE ULK1; RAB5C PROTEIN, HUMAN;

AUTOLYSOSOME; AUTOPHAGOSOME; AUTOPHAGY; EHRLICHIA CHAFFEENSIS; ENDOSOME; GENE TRANSLOCATION; INNATE IMMUNITY; LEGIONELLA; LISTERIA; LYSOSOME; MULTIVESICULAR BODY; MYCOBACTERIUM; NONHUMAN; REVIEW; SHIGELLA; STREPTOCOCCUS; ANIMAL; EHRLICHIOSIS; HOST PARASITE INTERACTION; HUMAN; METABOLISM; MICROBIOLOGY; PATHOLOGY; PHYSIOLOGY; TYPE IV SECRETION SYSTEM;

ANIMALS; AUTOPHAGIC CELL DEATH; CLASS III PHOSPHATIDYLINOSITOL 3-KINASES; EHRLICHIA CHAFFEENSIS; EHRLICHIOSIS; ENDOSOMES; HOST-PARASITE INTERACTIONS; HUMANS; LYSOSOMES; RAB5 GTP-BINDING PROTEINS; TYPE IV SECRETION SYSTEMS;

EID: 85070195487     PISSN: 21541248     EISSN: 21541256     Source Type: Journal    
DOI: 10.1080/21541248.2017.1332506     Document Type: Review

References (53)

1. Pfeffer SR. Rab GTPases: Master regulators that establish the secretory and endocytic pathways. Mol Biol Cell 2017; 28:712-5; PMID:28292916; https://doi.org/10.1091/mbc.E16-10-0737
2. Zhen Y, Stenmark H. Cellular functions of Rab GTPases at a glance. J Cell Sci 2015; 128:3171-6; PMID:26272922; https://doi.org/10.1242/jcs.166074
3. Fratti RA, Chua J, Vergne I, Deretic V. Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. Proc Natl Acad Sci U S A 2003; 100:5437-42; PMID:12702770; https://doi.org/10.1073/pnas.0737613100
4. Puri RV, Reddy PV, Tyagi AK. Secreted acid phosphatase (SapM) of Mycobacterium tuberculosis is indispensable for arresting phagosomal maturation and growth of the pathogen in guinea pig tissues. PloS One 2013; 8:e70514; PMID:23923000; https://doi.org/10.1371/journal.pone.0070514
5. Alvarez-Dominguez C, Madrazo-Toca F, Fernandez-Prieto L, Vandekerckhove J, Pareja E, Tobes R, Gomez-Lopez MT, Del Cerro-Vadillo E, Fresno M, Leyva-Cobián F, et al. Characterization of a Listeria monocytogenes protein interfering with Rab5a. Traffic 2008; 9:325-37; PMID:18088303; https://doi.org/10.1111/j.1600-0854.2007.00683.x
6. Mukherjee K, Parashuraman S, Raje M, Mukhopadhyay A. SopE acts as an Rab5-specific nucleotide exchange factor and recruits non-prenylated Rab5 on Salmonella-containing phagosomes to promote fusion with early endosomes. J Biol Chem 2001; 276:23607-15; PMID:11316807; https://doi.org/10.1074/jbc.M101034200
7. Mallo GV, Espina M, Smith AC, Terebiznik MR, Aleman A, Finlay BB, Rameh LE, Grinstein S, Brumell JH. SopB promotes phosphatidylinositol 3-phosphate formation on salmonella vacuoles by recruiting Rab5 and Vps34. J Cell Biol 2008; 182:741-52; PMID:18725540; https://doi.org/10.1083/jcb.200804131
8. Rikihisa Y. Molecular pathogenesis of Ehrlichia chaffeensis infection. Annu Rev Microbiol 2015; 69:283-304; PMID:26488275; https://doi.org/10.1146/annurev-micro-091014-104411
9. Mohan Kumar D, Yamaguchi M, Miura K, Lin M, Los M, Coy JF, Rikihisa Y. Ehrlichia chaffeensis uses its surface protein EtpE to bind GPI-anchored protein DNase X and trigger entry into mammalian cells. PLoS Pathog 2013; 9:e1003666; PMID:24098122; https://doi.org/10.1371/journal.ppat.1003666
10. Barnewall RE, Rikihisa Y, Lee EH. Ehrlichia chaffeensis inclusions are early endosomes which selectively accumulate transferrin receptor. Infect Immun 1997; 65:1455-61; PMID:9119487
11. Lin M, Liu H, Xiong Q, Niu H, Cheng Z, Yamamoto A, Rikihisa Y. Ehrlichia secretes Etf-1 to induce autophagy and capture nutrients for its growth through RAB5 and class III phosphatidylinositol 3-kinase. Autophagy 2016; 12:2145-66; PMID:27541856; https://doi.org/10.1080/15548627.2016.1217369
12. Barr F, Lambright DG. Rab GEFs and GAPs. Curr Opin Cell Biol 2010; 22:461-70; PMID:20466531; https://doi.org/10.1016/j.ceb.2010.04.007
13. Abu Kwaik Y, Bumann D. Microbial quest for food in vivo: ‘Nutritional virulence’ as an emerging paradigm. Cell Microbiol 2013; 15:882-90; PMID:23490329; https://doi.org/10.1111/cmi.12138
14. Niu H, Yamaguchi M, Rikihisa Y. Subversion of cellular autophagy by Anaplasma phagocytophilum. Cell Microbiol 2008; 10:593-605; PMID:17979984; https://doi.org/10.1111/j.1462-5822.2007.01068.x
15. Niu H, Rikihisa Y. Ats-1: A novel bacterial molecule that links autophagy to bacterial nutrition. Autophagy 2013; 9:787-8; PMID:23388398; https://doi.org/10.4161/auto.23693
16. Niu H, Xiong Q, Yamamoto A, Hayashi-Nishino M, Rikihisa Y. Autophagosomes induced by a bacterial Beclin 1 binding protein facilitate obligatory intracellular infection. Proc Natl Acad Sci U S A 2012; 109:20800-7; PMID:23197835; https://doi.org/10.1073/pnas.1218674109
17. Yang Z, Klionsky DJ. Eaten alive: A history of macroautophagy. Nat Cell Biol 2010; 12:814-22; PMID:20811353; https://doi.org/10.1038/ncb0910-814
18. Mizushima N, Komatsu M. Autophagy: Renovation of cells and tissues. Cell 2011; 147:728-41; PMID:22078875; https://doi.org/10.1016/j.cell.2011.10.026
19. Thurston TL, Ryzhakov G, Bloor S, von Muhlinen N, Randow F. The TBK1 adaptor and autophagy receptor NDP52 restricts the proliferation of ubiquitin-coated bacteria. Nat Immunol 2009; 10:1215-21; PMID:19820708; https://doi.org/10.1038/ni.1800
20. Yoshikawa Y, Ogawa M, Hain T, Yoshida M, Fukumatsu M, Kim M, Mimuro H, Nakagawa I, Yanagawa T, Ishii T, et al. Listeria monocytogenes ActA-mediated escape from autophagic recognition. Nat Cell Biol 2009; 11:1233-40; PMID:19749745; https://doi.org/10.1038/ncb1967
21. Dupont N, Lacas-Gervais S, Bertout J, Paz I, Freche B, Van Nhieu GT, van der Goot FG, Sansonetti PJ, Lafont F. Shigella phagocytic vacuolar membrane remnants participate in the cellular response to pathogen invasion and are regulated by autophagy. Cell Host Microbe 2009; 6:137-49; PMID:19683680; https://doi.org/10.1016/j.chom.2009.07.005
22. Zheng YT, Shahnazari S, Brech A, Lamark T, Johansen T, Brumell JH. The adaptor protein p62/SQSTM1 targets invading bacteria to the autophagy pathway. J Immunol 2009; 183:5909-16; PMID:19812211; https://doi.org/10.4049/jimmunol.0900441
23. Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, Deretic V. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 2004; 119:753-66; PMID:15607973; https://doi.org/10.1016/j.cell.2004.11.038
24. Homer CR, Richmond AL, Rebert NA, Achkar JP, McDonald C. ATG16L1 and NOD2 interact in an autophagy-dependent antibacterial pathway implicated in Crohn's disease pathogenesis. Gastroenterology 2010; 139:1630-41. 41 e1-2; PMID:20637199; https://doi.org/10.1053/j.gastro.2010.07.006
25. Itakura E, Kishi C, Inoue K, Mizushima N. Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol Biol Cell 2008; 19:5360-72; PMID:18843052; https://doi.org/10.1091/mbc.E08-01-0080
26. Russell RC, Tian Y, Yuan H, Park HW, Chang YY, Kim J, Kim H, Neufeld TP, Dillin A, Guan KL. ULK1 induces autophagy by phosphorylating Beclin-1 and activating VPS34 lipid kinase. Nat Cell Biol 2013; 15:741-50; PMID:23685627; https://doi.org/10.1038/ncb2757
27. Kim J, Kundu M, Viollet B, Guan KL. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol 2011; 13:132-41; PMID:21258367; https://doi.org/10.1038/ncb2152
28. Kim PK, Hailey DW, Mullen RT, Lippincott-Schwartz J. Ubiquitin signals autophagic degradation of cytosolic proteins and peroxisomes. Proc Natl Acad Sci U S A 2008; 105:20567-74; PMID:19074260; https://doi.org/10.1073/pnas.0810611105
29. Ichimura Y, Kumanomidou T, Sou YS, Mizushima T, Ezaki J, Ueno T, Kominami E, Yamane T, Tanaka K, Komatsu M. Structural basis for sorting mechanism of p62 in selective autophagy. J Biol Chem 2008; 283:22847-57; PMID:18524774; https://doi.org/10.1074/jbc.M802182200
30. Fujita N, Morita E, Itoh T, Tanaka A, Nakaoka M, Osada Y, Umemoto T, Saitoh T, Nakatogawa H, Kobayashi S, et al. Recruitment of the autophagic machinery to endosomes during infection is mediated by ubiquitin. J Cell Biol 2013; 203:115-28; PMID:24100292; https://doi.org/10.1083/jcb.201304188
31. Barnett TC, Liebl D, Seymour LM, Gillen CM, Lim JY, Larock CN, Davies MR, Schulz BL, Nizet V, Teasdale RD, et al. The globally disseminated M1T1 clone of group A Streptococcus evades autophagy for intracellular replication. Cell Host Microbe 2013; 14:675-82; PMID:24331465; https://doi.org/10.1016/j.chom.2013.11.003
32. Khweek AA, Caution K, Akhter A, Abdulrahman BA, Tazi M, Hassan H, Majumdar N, Doran A, Guirado E, Schlesinger LS, et al. A bacterial protein promotes the recognition of the Legionella pneumophila vacuole by autophagy. Eur J Immunol 2013; 43:1333-44; PMID:23420491; https://doi.org/10.1002/eji.201242835
33. Rikihisa Y, Lin M. Anaplasma phagocytophilum and Ehrlichia chaffeensis type IV secretion and Ank proteins. Curr Opin Microbiol 2010; 13:59-66; PMID:20053580; https://doi.org/10.1016/j.mib.2009.12.008
34. Backert S, Meyer TF. Type IV secretion systems and their effectors in bacterial pathogenesis. Curr Opin Microbiol 2006; 9:207-17; PMID:16529981; https://doi.org/10.1016/j.mib.2006.02.008
35. Berg TO, Fengsrud M, Stromhaug PE, Berg T, Seglen PO. Isolation and characterization of rat liver amphisomes. Evidence for fusion of autophagosomes with both early and late endosomes. J Biol Chem 1998; 273:21883-92; PMID:9705327; https://doi.org/10.1074/jbc.273.34.21883
36. Dou Z, Pan JA, Dbouk HA, Ballou LM, Deleon JL, Fan Y, Chen JS, Liang Z, Li G, Backer JM, et al. Class IA PI3K p110beta subunit promotes autophagy through Rab5 small GTPase in response to growth factor limitation. Mol Cell 2013; 50:29-42; PMID:23434372; https://doi.org/10.1016/j.molcel.2013.01.022
37. Su WC, Chao TC, Huang YL, Weng SC, Jeng KS, Lai MM. Rab5 and class III phosphoinositide 3-kinase Vps34 are involved in hepatitis C virus NS4B-induced autophagy. J Virol 2011; 85:10561-71; PMID:21835792; https://doi.org/10.1128/JVI.00173-11
38. Ravikumar B, Imarisio S, Sarkar S, O'Kane CJ, Rubinsztein DC. Rab5 modulates aggregation and toxicity of mutant huntingtin through macroautophagy in cell and fly models of Huntington disease. J Cell Sci 2008; 121:1649-60; PMID:18430781; https://doi.org/10.1242/jcs.025726
39. Venkatraman P, Wetzel R, Tanaka M, Nukina N, Goldberg AL. Eukaryotic proteasomes cannot digest polyglutamine sequences and release them during degradation of polyglutamine-containing proteins. Mol Cell 2004; 14:95-104; PMID:15068806; https://doi.org/10.1016/S1097-2765(04)00151-0
40. Raspe M, Gillis J, Krol H, Krom S, Bosch K, van Veen H, Reits E. Mimicking proteasomal release of polyglutamine peptides initiates aggregation and toxicity. J Cell Sci 2009; 122:3262-71; PMID:19690053; https://doi.org/10.1242/jcs.045567
41. Pal A, Severin F, Lommer B, Shevchenko A, Zerial M. Huntingtin-HAP40 complex is a novel Rab5 effector that regulates early endosome motility and is up-regulated in Huntington's disease. J Cell Biol 2006; 172:605-18; PMID:16476778; https://doi.org/10.1083/jcb.200509091
42. Li Y, Zhao Y, Hu J, Xiao J, Qu L, Wang Z, Ma D, Chen Y. A novel ER-localized transmembrane protein, EMC6, interacts with RAB5A and regulates cell autophagy. Autophagy 2013; 9:150-63; PMID:23182941; https://doi.org/10.4161/auto.22742
43. Nakatsukasa K, Kanada A, Matsuzaki M, Byrne SD, Okumura F, Kamura T. The nutrient stress-induced small GTPase Rab5 contributes to the activation of vesicle trafficking and vacuolar activity. J Biol Chem 2014; 289:20970-8; PMID:24923442; https://doi.org/10.1074/jbc.M114.548297
44. Kern A, Dikic I, Behl C. The integration of autophagy and cellular trafficking pathways via RAB GAPs. Autophagy 2015; 11:2393-7; PMID:26565612; https://doi.org/10.1080/15548627.2015.1110668
45. Lamb CA, Longatti A, Tooze SA. Rabs and GAPs in starvation-induced autophagy. Small GTPases 2016; 7:265-9; PMID:27669114; https://doi.org/10.1080/21541248.2016.1220779
46. Sneve ML, Overbye A, Fengsrud M, Seglen PO. Comigration of two autophagosome-associated dehydrogenases on two-dimensional polyacrylamide gels. Autophagy 2005; 1:157-62; PMID:16874067; https://doi.org/10.4161/auto.1.3.2037
47. Morvan J, Kochl R, Watson R, Collinson LM, Jefferies HB, Tooze SA. In vitro reconstitution of fusion between immature autophagosomes and endosomes. Autophagy 2009; 5:676-89; PMID:19337031; https://doi.org/10.4161/auto.5.5.8378
48. Tooze J, Hollinshead M, Ludwig T, Howell K, Hoflack B, Kern H. In exocrine pancreas, the basolateral endocytic pathway converges with the autophagic pathway immediately after the early endosome. J Cell Biol 1990; 111:329-45; PMID:2166050; https://doi.org/10.1083/jcb.111.2.329
49. Eskelinen EL. Maturation of autophagic vacuoles in mammalian cells. Autophagy 2005; 1:1-10; PMID:16874026; https://doi.org/10.4161/auto.1.1.1270
50. Fader CM, Colombo MI. Autophagy and multivesicular bodies: Two closely related partners. Cell Death Differ 2009; 16:70-8; PMID:19008921; https://doi.org/10.1038/cdd.2008.168
51. Shin HW, Hayashi M, Christoforidis S, Lacas-Gervais S, Hoepfner S, Wenk MR, Modregger J, Uttenweiler-Joseph S, Wilm M, Nystuen A, et al. An enzymatic cascade of Rab5 effectors regulates phosphoinositide turnover in the endocytic pathway. J Cell Biol 2005; 170:607-18; PMID:16103228; https://doi.org/10.1083/jcb.200505128
52. Vieira OV, Botelho RJ, Rameh L, Brachmann SM, Matsuo T, Davidson HW, Schreiber A, Backer JM, Cantley LC, Grinstein S. Distinct roles of class I and class III phosphatidylinositol 3-kinases in phagosome formation and maturation. J Cell Biol 2001; 155:19-25; PMID:11581283; https://doi.org/10.1083/jcb.200107069
53. Gillooly DJ, Morrow IC, Lindsay M, Gould R, Bryant NJ, Gaullier JM, Parton RG, Stenmark H. Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J 2000; 19:4577-88; PMID:10970851; https://doi.org/10.1093/emboj/19.17.4577