Correlative light and electron microscopy imaging of autophagy in a zebrafish infection model

Autophagy

Volumn 10, Issue 10, 2014, Pages 1844-1857

  Hosseini, Rohola ^a   Lamers, Gerda E M ^a   Hodzic, Zlatan ^a   Meijer, Annemarie H ^a   Schaaf, Marcel J M ^a   Spaink, Herman P ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

Author keywords

Autophagic vacuole; Confocal laser scanning microscopy; Correlative; Imaging; Infection; Mycobacterium; Tail fin; TEM; Zebrafish

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGY; CELL STRUCTURE; CELL VACUOLE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; DISEASE TRANSMISSION; ELECTRON MICROSCOPY; EMBRYO; GRANULOMA; IN VIVO STUDY; LARVA; LEUKOCYTE; LYSOSOME; MYCOBACTERIOSIS; MYCOBACTERIUM MARINUM; NONHUMAN; PHAGOSOME; TAIL; ZEBRA FISH; ANIMAL; CONFOCAL MICROSCOPY; DISEASE MODEL; FIN (ORGAN); METABOLISM; MICROBIOLOGY; MYCOBACTERIUM INFECTIONS, NONTUBERCULOUS; PATHOLOGY; PHYSIOLOGY; PROCEDURES; ULTRASTRUCTURE;

DANIO RERIO; MYCOBACTERIUM;

GREEN FLUORESCENT PROTEIN; LC3 PROTEIN, ZEBRAFISH; MICROTUBULE ASSOCIATED PROTEIN; ZEBRAFISH PROTEIN;

ANIMAL FINS; ANIMALS; AUTOPHAGY; DISEASE MODELS, ANIMAL; GREEN FLUORESCENT PROTEINS; LARVA; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; MICROTUBULE-ASSOCIATED PROTEINS; MYCOBACTERIUM INFECTIONS, NONTUBERCULOUS; MYCOBACTERIUM MARINUM; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84907891738     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.29992     Document Type: Article

References (58)

1. Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature 2008; 451:1069-75; PMID:18305538; http://dx.doi.org/10.1038/nature06639
2. Dunn WA Jr. Studies on the mechanisms of autophagy: formation of the autophagic vacuole. J Cell Biol 1990; 110:1923-33; PMID:2351689; http://dx.doi.org/10.1083/jcb.110.6.1923
3. Dunn WA Jr. Studies on the mechanisms of autophagy: maturation of the autophagic vacuole. J Cell Biol 1990; 110:1935-45; PMID:2161853; http://dx.doi.org/10.1083/jcb.110.6.1935
4. Yang Z, Klionsky DJ. Eaten alive: a history of macroautophagy. Nat Cell Biol 2010; 12:814-22; PMID:20811353; http://dx.doi.org/10.1038/ncb0910-814
5. Eskelinen E-L. New insights into the mechanisms of macroautophagy in mammalian cells. Int Rev Cell Mol Biol 2008; 266:207-47; PMID:18544495; http://dx.doi.org/10.1016/S1937-6448(07)66005-5
6. Kraft C, Peter M, Hofmann K. Selective autophagy: ubiquitin-mediated recognition and beyond. Nat Cell Biol 2010; 12:836-41; PMID:20811356; http://dx.doi.org/10.1038/ncb0910-836
7. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000; 19:5720-8; PMID:11060023; http://dx.doi.org/10.1093/emboj/19.21.5720
8. Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 2004; 15:1101-11; PMID:14699058; http://dx.doi.org/10.1091/mbc.E03-09-0704
9. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8:445-544; PMID:22966490; http://dx.doi.org/10.4161/auto.19496
10. Nakagawa I, Amano A, Mizushima N, Yamamoto A, Yamaguchi H, Kamimoto T, Nara A, Funao J, Nakata M, Tsuda K, et al. Autophagy defends cells against invading group A Streptococcus. Science 2004; 306:1037-40; PMID:15528445; http://dx.doi.org/10.1126/science.1103966
11. 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; http://dx.doi.org/10.1016/j.cell.2004.11.038
12. Levine B, Mizushima N, Virgin HW. Autophagy in immunity and inflammation. Nature 2011; 469:323-35; PMID:21248839; http://dx.doi.org/10.1038/nature09782
13. Deretic V. Multiple regulatory and effector roles of autophagy in immunity. Curr Opin Immunol 2009; 21:53-62; PMID:19269148; http://dx.doi.org/10.1016/j.coi.2009.02.002
14. Kuballa P, Nolte WM, Castoreno AB, Xavier RJ. Autophagy and the immune system. Annu Rev Immunol 2012; 30:611-46; PMID:22449030; http://dx.doi.org/10.1146/annurev-immunol-020711-074948
15. Armstrong JA, Hart PD. Response of cultured macrophages to Mycobacterium tuberculosis, with observations on fusion of lysosomes with phagosomes. J Exp Med 1971; 134:713-40; PMID:15776571; http://dx.doi.org/10.1084/jem.134.3.713
16. Russell DG. Who puts the tubercle in tuberculosis? Nat Rev Microbiol 2007; 5:39-47; PMID:17160001; http://dx.doi.org/10.1038/nrmicro1538
17. van der Wel N, Hava D, Houben D, Fluitsma D, van Zon M, Pierson J, Brenner M, Peters PJ. M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 2007; 129:1287-98; PMID:17604718; http://dx.doi.org/10.1016/j.cell.2007.05.059
18. Houben D, Demangel C, van Ingen J, Perez J, Baldeón L, Abdallah AM, Caleechurn L, Bottai D, van Zon M, de Punder K, et al. ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria. Cell Microbiol 2012; 14:1287-98; PMID:22524898; http://dx.doi.org/10.1111/j.1462-5822.2012.01799.x
19. Watson RO, Manzanillo PS, Cox JS. Extracellular M. tuberculosis DNA targets bacteria for autophagy by activating the host DNA-sensing pathway. Cell 2012; 150:803-15; PMID:22901810; http://dx.doi.org/10.1016/j.cell.2012.06.040
20. Fabri M, Stenger S, Shin D-M, Yuk J-M, Liu PT, Realegeno S, Lee H-M, Krutzik SR, Schenk M, Sieling PA, et al. Vitamin D is required for IFN-gamma-mediated antimicrobial activity of human macrophages. Sci Transl Med 2011; 3:ra102; PMID:21998409; http://dx.doi.org/10.1126/scitranslmed.3003045
21. Bradfute SB, Castillo EF, Arko-Mensah J, Chauhan S, Jiang S, Mandell M, Deretic V. Autophagy as an immune effector against tuberculosis. Curr Opin Microbiol 2013; 16:355-65; PMID:23790398; http://dx.doi.org/10.1016/j.mib.2013.05.003
22. th, Kyei GB, Johansen T, Vergne I, et al. Delivery of cytosolic components by autophagic adaptor protein p62 endows autophagosomes with unique antimicrobial properties. Immunity 2010; 32:329-41; PMID:20206555; http://dx.doi.org/10.1016/j.immuni.2010.02.009
23. Alonso S, Pethe K, Russell DG, Purdy GE. Lysosomal killing of Mycobacterium mediated by ubiquitin-derived peptides is enhanced by autophagy. Proc Natl Acad Sci U S A 2007; 104:6031-6; PMID:17389386; http://dx.doi.org/10.1073/pnas.0700036104
24. Dowling JJ, Low SE, Busta AS, Feldman EL. Zebrafish MTMR14 is required for excitation-contraction coupling, developmental motor function and the regulation of autophagy. Hum Mol Genet 2010; 19:2668-81; PMID:20400459; http://dx.doi.org/10.1093/hmg/ddq153
25. Fleming A, Rubinsztein DC. Zebrafish as a model to understand autophagy and its role in neurological disease. Biochim Biophys Acta 2011; 1812:520-6; PMID:21256213; http://dx.doi.org/10.1016/j.bbadis.2011.01.004
26. Boglev Y, Badrock AP, Trotter AJ, Du Q, Richardson EJ, Parslow AC, Markmiller SJ, Hall NE, de Jong-Curtain TA, Ng AY, et al. Autophagy induction is a Tor- and Tp53-independent cell survival response in a zebrafish model of disrupted ribosome biogenesis. PLoS Genet 2013; 9:e1003279; PMID:23408911; http://dx.doi.org/10.1371/journal.pgen.1003279
27. Meeker ND, Trede NS. Immunology and zebrafish: spawning new models of human disease. Dev Comp Immunol 2008; 32:745-57; PMID:18222541; http://dx.doi.org/10.1016/j.dci.2007.11.011
28. Hu Z, Zhang J, Zhang Q. Expression pattern and functions of autophagy-related gene atg5 in zebrafish organogenesis. Autophagy 2011; 7:1514-27; PMID:22082871; http://dx.doi.org/10.4161/auto.7.12.18040
29. Benato F, Skobo T, Gioacchini G, Moro I, Ciccosanti F, Piacentini M, Fimia GM, Carnevali O, Dalla Valle L. Ambra1 knockdown in zebrafish leads to incomplete development due to severe defects in organogenesis. Autophagy 2013; 9:476-95; PMID:23348054; http://dx.doi.org/10.4161/auto.23278
30. Wager K, Russell C. Mitophagy and neurodegeneration: the zebrafish model system. Autophagy 2013; 9:1693-709; PMID:23939015; http://dx.doi.org/10.4161/auto.25082
31. Mostowy S, Boucontet L, Mazon Moya MJ, Sirianni A, Boudinot P, Hollinshead M, Cossart P, Herbomel P, Levraud J-P, Colucci-Guyon E. The zebrafish as a new model for the in vivo study of Shigella flexneri interaction with phagocytes and bacterial autophagy. PLoS Pathog 2013; 9:e1003588; PMID:24039575; http://dx.doi.org/10.1371/journal.ppat.1003588
32. He C, Bartholomew CR, Zhou W, Klionsky DJ. Assaying autophagic activity in transgenic GFP-Lc3 and GFP-Gabarap zebrafish embryos. Autophagy 2009; 5:520-6; PMID:19221467; http://dx.doi.org/10.4161/auto.5.4.7768
33. van der Vaart M, Spaink HP, Meijer AH. Pathogen recognition and activation of the innate immune response in zebrafish. Adv Hematol 2012; 2012:159807; PMID:22811714; http://dx.doi.org/10.1155/2012/159807
34. Hanson HH, Kang S, Fernández-Monreal M, Oung T, Yildirim M, Lee R, Suyama K, Hazan RB, Phillips GR. LC3-dependent intracellular membrane tubules induced by gamma-protocadherins A3 and B2: a role for intraluminal interactions. J Biol Chem 2010; 285:20982-92; PMID:20439459; http://dx.doi.org/10.1074/jbc.M109.092031
35. Lai SC, Devenish RJ. LC3-Associated Phagocytosis (LAP): Connections with Host Autophagy. Cells 2012; 1:396-408; PMID:24710482; http://dx.doi. org/10.3390/cells1030396
36. Sanjuan MA, Dillon CP, Tait SWG, Moshiach S, Dorsey F, Connell S, Komatsu M, Tanaka K, Cleveland JL, Withoff S, et al. Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 2007; 450:1253-7; PMID:18097414; http://dx.doi.org/10.1038/nature06421
37. Florey O, Kim SE, Sandoval CP, Haynes CM, Overholtzer M. Autophagy machinery mediates macroendocytic processing and entotic cell death by targeting single membranes. Nat Cell Biol 2011; 13:1335-43; PMID:22002674; http://dx.doi.org/10.1038/ncb2363
38. Tobin DM, Ramakrishnan L. Comparative pathogenesis of Mycobacterium marinum and Mycobacterium tuberculosis. Cell Microbiol 2008; 10:1027-39; PMID:18298637; http://dx.doi.org/10.1111/j.1462-5822.2008.01133.x
39. Stamm LM, Brown EJ. Mycobacterium marinum: the generalization and specialization of a pathogenic mycobacterium. Microbes Infect 2004; 6:1418-28; PMID:15596129; http://dx.doi.org/10.1016/j.micinf.2004.10.003
40. Berg RD, Ramakrishnan L. Insights into tuberculosis from the zebrafish model. Trends Mol Med 2012; 18:689-90; PMID:23084762; http://dx.doi.org/10.1016/j.molmed.2012.10.002
41. Stamm LM, Morisaki JH, Gao L-Y, Jeng RL, McDonald KL, Roth R, Takeshita S, Heuser J, Welch MD, Brown EJ. Mycobacterium marinum escapes from phagosomes and is propelled by actin-based motility. J Exp Med 2003; 198:1361-8; PMID:14597736; http://dx.doi.org/10.1084/jem.20031072
42. Benard EL, van der Sar AM, Ellett F, Lieschke GJ, Spaink HP, Meijer AH. Infection of zebrafish embryos with intracellular bacterial pathogens. J Vis Exp 2012; •••:3781; PMID:22453760
43. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. Stages of embryonic development of the zebrafish. Dev Dyn 1995; 203:253-310; PMID:8589427; http://dx.doi.org/10.1002/aja.1002030302
44. Cooper MS, Szeto DP, Sommers-Herivel G, Topczewski J, Solnica-Krezel L, Kang H-C, Johnson I, Kimelman D. Visualizing morphogenesis in transgenic zebrafish embryos using BODIPY TR methyl ester dye as a vital counterstain for GFP. Dev Dyn 2005; 232:359-68; PMID:15614774; http://dx.doi.org/10.1002/dvdy.20252
45. Meijer AH, Spaink HP. Host-pathogen interactions made transparent with the zebrafish model. Curr Drug Targets 2011; 12:1000-17; PMID:21366518; http://dx.doi.org/10.2174/138945011795677809
46. Renshaw SA, Loynes CA, Trushell DMI, Elworthy S, Ingham PW, Whyte MKB. A transgenic zebrafish model of neutrophilic inflammation. Blood 2006; 108:3976-8; PMID:16926288; http://dx.doi.org/10.1182/blood-2006-05-024075
47. Mathias JR, Dodd ME, Walters KB, Yoo SK, Ranheim EA, Huttenlocher A. Characterization of zebrafish larval inflammatory macrophages. Dev Comp Immunol 2009; 33:1212-7; PMID:19619578; http://dx.doi.org/10.1016/j.dci.2009.07.003
48. Pozos TC, Ramakrishnan L, Ramakrishan L. New models for the study of Mycobacterium-host interactions. Curr Opin Immunol 2004; 16:499-505; PMID:15245746; http://dx.doi.org/10.1016/j.coi.2004.05.011
49. McLaughlin B, Chon JS, MacGurn JA, Carlsson F, Cheng TL, Cox JS, Brown EJ. A mycobacterium ESX-1-secreted virulence factor with unique requirements for export. PLoS Pathog 2007; 3:e105; PMID:17676952; http://dx.doi.org/10.1371/journal.ppat.0030105
50. Lerena MC, Colombo MI. Mycobacterium marinum induces a marked LC3 recruitment to its containing phagosome that depends on a functional ESX-1 secretion system. Cell Microbiol 2011; 13:814-35; PMID:21447143; http://dx.doi.org/10.1111/j.1462-5822.2011.01581.x
51. Sanjuan MA, Milasta S, Green DR. Toll-like receptor signaling in the lysosomal pathways. Immunol Rev 2009; 227:203-20; PMID:19120486; http://dx.doi.org/10.1111/j.1600-065X.2008.00732.x
52. Mostowy S. Autophagy and bacterial clearance: a not so clear picture. Cell Microbiol 2013; 15:395-402; PMID:23121192; http://dx.doi.org/10.1111/cmi.12063
53. Ponpuak M, Deretic V. Autophagy and p62/sequestosome 1 generate neo-antimicrobial peptides (cryptides) from cytosolic proteins. Autophagy 2011; 7:336-7; PMID:21187720; http://dx.doi.org/10.4161/auto.7.3.14500
54. Pfeifer U. Inhibition by insulin of the formation of autophagic vacuoles in rat liver. A morphometric approach to the kinetics of intracellular degradation by autophagy. J Cell Biol 1978; 78:152-67; PMID:670291; http://dx.doi.org/10.1083/jcb.78.1.152
55. Schworer CM, Shiffer KA, Mortimore GE. Quantitative relationship between autophagy and proteolysis during graded amino acid deprivation in perfused rat liver. J Biol Chem 1981; 256:7652-8; PMID:7019210
56. Rubinsztein DC, Codogno P, Levine B. Autophagy modulation as a potential therapeutic target for diverse diseases. Nat Rev Drug Discov 2012; 11:709-30; PMID:22935804; http://dx.doi.org/10.1038/nrd3802
57. Strack RL, Hein B, Bhattacharyya D, Hell SW, Keenan RJ, Glick BS. A rapidly maturing far-red derivative of DsRed-Express2 for whole-cell labeling. Biochemistry 2009; 48:8279-81; PMID:19658435; http://dx.doi.org/10.1021/bi900870u
58. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods 2012; 9:676-82; PMID:22743772; http://dx.doi.org/10.1038/nmeth.2019