Cytoplasmic Actin Is an Extracellular Insect Immune Factor which Is Secreted upon Immune Challenge and Mediates Phagocytosis and Direct Killing of Bacteria, and Is a Antagonist
Actin is one of the best studied, evolutionary conserved and most abundant intracellular proteins. Actin can exists in globular and filamentous functionally distinct forms, and is involved in a variety of biological processes, such as muscle contraction, cell motility, cell division, vesicle and organelle movement, endocytosis, and cell signaling. Here we show a novel function of insect cytoplasmic actin, as an extracellular immune factor. Actin is externalized by insect immune competent cells upon immune challenge with bacteria or bacterial surface components, and once externalized, actin binds with high affinity to the surface of bacteria. A functional role of actin’s interaction with bacteria is to mediate their killing through either phagocytosis or direct antibacterial action. The globular and filamentous forms of actins appear to play distinct functions as extracellular immune factors. Actin also plays a role as a Plasmodium antagonist as it limits parasite infection of the mosquito gut tissue.
Vyšlo v časopise:
Cytoplasmic Actin Is an Extracellular Insect Immune Factor which Is Secreted upon Immune Challenge and Mediates Phagocytosis and Direct Killing of Bacteria, and Is a Antagonist. PLoS Pathog 11(2): e32767. doi:10.1371/journal.ppat.1004631
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1004631
Souhrn
Actin is one of the best studied, evolutionary conserved and most abundant intracellular proteins. Actin can exists in globular and filamentous functionally distinct forms, and is involved in a variety of biological processes, such as muscle contraction, cell motility, cell division, vesicle and organelle movement, endocytosis, and cell signaling. Here we show a novel function of insect cytoplasmic actin, as an extracellular immune factor. Actin is externalized by insect immune competent cells upon immune challenge with bacteria or bacterial surface components, and once externalized, actin binds with high affinity to the surface of bacteria. A functional role of actin’s interaction with bacteria is to mediate their killing through either phagocytosis or direct antibacterial action. The globular and filamentous forms of actins appear to play distinct functions as extracellular immune factors. Actin also plays a role as a Plasmodium antagonist as it limits parasite infection of the mosquito gut tissue.
Zdroje
1. Pollard TD, Cooper JA (2009) Actin, a central player in cell shape and movement. Science 326: 1208–1212. doi: 10.1126/science.1175862 19965462
2. Dominguez R, Holmes KC (2011) Actin structure and function. Annu Rev Biophys 40: 169–186. doi: 10.1146/annurev-biophys-042910-155359 21314430
3. May RC, Machesky LM (2001) Phagocytosis and the actin cytoskeleton. J Cell Sci 114: 1061–1077. 11228151
4. Zhang JG, Czabotar PE, Policheni AN, Caminschi I, Wan SS, et al. (2012) The dendritic cell receptor Clec9A binds damaged cells via exposed actin filaments. Immunity 36: 646–657. doi: 10.1016/j.immuni.2012.03.009 22483802
5. Ahrens S, Zelenay S, Sancho D, Hanc P, Kjaer S, et al. (2012) F-actin is an evolutionarily conserved damage-associated molecular pattern recognized by DNGR-1, a receptor for dead cells. Immunity 36: 635–645. doi: 10.1016/j.immuni.2012.03.008 22483800
6. Salazar CE, Hamm DM, Wesson DM, Beard CB, Kumar V, et al. (1994) A cytoskeletal actin gene in the mosquito Anopheles gambiae. Insect Mol Biol 3: 1–13. doi: 10.1111/j.1365-2583.1994.tb00145.x 8069411
7. Vierstraete E, Cerstiaens A, Baggerman G, Van den Bergh G, De Loof A, et al. (2003) Proteomics in Drosophila melanogaster: first 2D database of larval hemolymph proteins. Biochem Biophys Res Commun 304: 831–838. doi: 10.1016/S0006-291X(03)00683-1 12727233
8. Agiesh Kumar B, Paily KP (2008) Actin protein up-regulated upon infection and development of the filarial parasite, Wuchereria bancrofti (Spirurida: Onchocercidae), in the vector mosquito, Culex quinquefasciatus (Diptera: Culicidae). Exp Parasitol 118: 297–302. doi: 10.1016/j.exppara.2007.08.012 17931628
9. Paskewitz SM, Shi L (2005) The hemolymph proteome of Anopheles gambiae. Insect Biochem Mol Biol 35: 815–824. doi: 10.1016/j.ibmb.2005.03.002 15944078
10. Vierstraete E, Verleyen P, Baggerman G, D′Hertog W, Van den Bergh G, et al. (2004) A proteomic approach for the analysis of instantly released wound and immune proteins in Drosophila melanogaster hemolymph. Proc Natl Acad Sci U S A 101: 470–475. doi: 10.1073/pnas.0304567101 14707262
11. Kadiu I, Ricardo-Dukelow M, Ciborowski P, Gendelman HE (2007) Cytoskeletal protein transformation in HIV-1-infected macrophage giant cells. J Immunol 178: 6404–6415. doi: 10.4049/jimmunol.178.10.6404 17475870
12. Chertova E, Chertov O, Coren LV, Roser JD, Trubey CM, et al. (2006) Proteomic and biochemical analysis of purified human immunodeficiency virus type 1 produced from infected monocyte-derived macrophages. J Virol 80: 9039–9052. doi: 10.1128/JVI.01013-06 16940516
13. Clayton AM, Dong Y, Dimopoulos G (2014) The Anopheles innate immune system in the defense against malaria infection. J Innate Immun 6: 169–181. doi: 10.1159/000353602 23988482
14. Cirimotich CM, Dong Y, Garver LS, Sim S, Dimopoulos G (2010) Mosquito immune defenses against Plasmodium infection. Dev Comp Immunol 34: 387–395. doi: 10.1016/j.dci.2009.12.005 20026176
15. Dong Y, Dimopoulos G (2009) Anopheles fibrinogen-related proteins provide expanded pattern recognition capacity against bacteria and malaria parasites. J Biol Chem 284: 9835–9844. doi: 10.1074/jbc.M807084200 19193639
16. Blandin S, Shiao SH, Moita LF, Janse CJ, Waters AP, et al. (2004) Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell 116: 661–670. doi: 10.1016/S0092-8674(04)00173-4 15006349
17. Dong Y, Aguilar R, Xi Z, Warr E, Mongin E, et al. (2006) Anopheles gambiae immune responses to human and rodent Plasmodium parasite species. PLoS Pathog 2: e52. doi: 10.1371/journal.ppat.0020052 16789837
18. Nagai Y, Akashi S, Nagafuku M, Ogata M, Iwakura Y, et al. (2002) Essential role of MD-2 in LPS responsiveness and TLR4 distribution. Nat Immunol 3: 667–672. 12055629
19. Viriyakosol S, Tobias PS, Kitchens RL, Kirkland TN (2001) MD-2 binds to bacterial lipopolysaccharide. J Biol Chem 276: 38044–38051. 11500507
20. Visintin A, Mazzoni A, Spitzer JA, Segal DM (2001) Secreted MD-2 is a large polymeric protein that efficiently confers lipopolysaccharide sensitivity to Toll-like receptor 4. Proc Natl Acad Sci U S A 98: 12156–12161. doi: 10.1073/pnas.211445098 11593030
21. Shi XZ, Zhong X, Yu XQ (2012) Drosophila melanogaster NPC2 proteins bind bacterial cell wall components and may function in immune signal pathways. Insect Biochem Mol Biol 42: 545–556. doi: 10.1016/j.ibmb.2012.04.002 22580186
22. Warr E, Das S, Dong Y, Dimopoulos G (2008) The Gram-negative bacteria-binding protein gene family: its role in the innate immune system of anopheles gambiae and in anti-Plasmodium defence. Insect Mol Biol 17: 39–51. doi: 10.1111/j.1365-2583.2008.00778.x 18237283
23. Dong Y, Taylor HE, Dimopoulos G (2006) AgDscam, a hypervariable immunoglobulin domain-containing receptor of the Anopheles gambiae innate immune system. PLoS Biol 4: e229. doi: 10.1371/journal.pbio.0040229 16774454
24. Levashina EA, Moita LF, Blandin S, Vriend G, Lagueux M, et al. (2001) Conserved role of a complement-like protein in phagocytosis revealed by dsRNA knockout in cultured cells of the mosquito, Anopheles gambiae. Cell 104: 709–718. doi: 10.1016/S0092-8674(01)00267-7 11257225
25. Fyrberg EA, Fyrberg CC, Biggs JR, Saville D, Beall CJ, et al. (1998) Functional nonequivalence of Drosophila actin isoforms. Biochem Genet 36: 271–287. doi: 10.1023/A:1018785127079 9791722
26. Wagner CR, Mahowald AP, Miller KG (2002) One of the two cytoplasmic actin isoforms in Drosophila is essential. Proc Natl Acad Sci U S A 99: 8037–8042. doi: 10.1073/pnas.082235499 12034866
27. Leulier F, Parquet C, Pili-Floury S, Ryu JH, Caroff M, et al. (2003) The Drosophila immune system detects bacteria through specific peptidoglycan recognition. Nat Immunol 4: 478–484. doi: 10.1038/ni922 12692550
28. Zhang M, Schekman R Cell biology. (2013) Unconventional secretion, unconventional solutions. Science 340: 559–561. doi: 10.1126/science.1234740 23641104
29. Malhotra V (2013) Unconventional protein secretion: an evolving mechanism. EMBO J 32: 1660–1664. doi: 10.1038/emboj.2013.104 23665917
30. Rabouille C, Malhotra V, Nickel W (2013) Diversity in unconventional protein secretion. J Cell Sci 125: 5251–5255. doi: 10.1242/jcs.103630
31. Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, et al. (2008) Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319: 1244–1247. doi: 10.1126/science.1153124 18309083
32. Carta S, Lavieri R, Rubartelli A Different Members of the IL-1 Family Come Out in Different Ways: DAMPs vs. Cytokines? Front Immunol 4: 123.
33. Osta MA, Christophides GK, Vlachou D, Kafatos FC (2004) Innate immunity in the malaria vector Anopheles gambiae: comparative and functional genomics. J Exp Biol 207: 2551–2563. doi: 10.1242/jeb.01066 15201288
34. Sun H, Bristow BN, Qu G, Wasserman SA (2002) A heterotrimeric death domain complex in Toll signaling. Proc Natl Acad Sci U S A 99: 12871–12876. doi: 10.1073/pnas.202396399 12351681
35. Dong Y, Cirimotich CM, Pike A, Chandra R, Dimopoulos G (2012) Anopheles NF-kappaB-regulated splicing factors direct pathogen-specific repertoires of the hypervariable pattern recognition receptor AgDscam. Cell Host Microbe 12: 521–530. doi: 10.1016/j.chom.2012.09.004 23084919
36. Ramet M, Pearson A, Manfruelli P, Li X, Koziel H, et al. (2001) Drosophila scavenger receptor CI is a pattern recognition receptor for bacteria. Immunity 15: 1027–1038. doi: 10.1016/S1074-7613(01)00249-7 11754822
37. Ramet M, Manfruelli P, Pearson A, Mathey-Prevot B, Ezekowitz RA (2002) Functional genomic analysis of phagocytosis and identification of a Drosophila receptor for E. coli. Nature 416: 644–648. doi: 10.1038/nature735
38. Dong Y, Manfredini F, Dimopoulos G (2009) Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathog 5: e1000423. doi: 10.1371/journal.ppat.1000423 19424427
39. Krusong K, Poolpipat P, Supungul P, Tassanakajon A (2012) A comparative study of antimicrobial properties of crustinPm1 and crustinPm7 from the black tiger shrimp Penaeus monodon. Dev Comp Immunol 36: 208–215. doi: 10.1016/j.dci.2011.08.002 21855569
40. Kaneko T, Goldman WE, Mellroth P, Steiner H, Fukase K, et al. (2004) Monomeric and polymeric gram-negative peptidoglycan but not purified LPS stimulate the Drosophila IMD pathway. Immunity 20: 637–649. doi: 10.1016/S1074-7613(04)00104-9 15142531
41. Henty-Ridilla JL, Shimono M, Li J, Chang JH, Day B, et al. (2013) The plant actin cytoskeleton responds to signals from microbe-associated molecular patterns. PLoS Pathog 9: e1003290. doi: 10.1371/journal.ppat.1003290 23593000
42. Shiao SH, Whitten MM, Zachary D, Hoffmann JA, Levashina EA (2006) Fz2 and cdc42 mediate melanization and actin polymerization but are dispensable for Plasmodium killing in the mosquito midgut. PLoS Pathog 2: e133. doi: 10.1371/journal.ppat.0020133 17196037
43. Schlegelmilch T, Vlachou D (2013) Cell biological analysis of mosquito midgut invasion: the defensive role of the actin-based ookinete hood. Pathog Glob Health 107: 480–492. doi: 10.1179/2047772413Z.000000000180 24428832
44. Blumenthal A, Ehlers S, Lauber J, Buer J, Lange C, et al. (2006) The Wingless homolog WNT5A and its receptor Frizzled-5 regulate inflammatory responses of human mononuclear cells induced by microbial stimulation. Blood 108: 965–973. doi: 10.1182/blood-2005-12-5046 16601243
45. Schmucker D, Chen B (2009) Dscam and DSCAM: complex genes in simple animals, complex animals yet simple genes. Genes Dev 23: 147–156. doi: 10.1101/gad.1752909 19171779
46. Valanne S, Wang JH, Ramet M (2011) The Drosophila Toll signaling pathway. J Immunol 186: 649–656. doi: 10.4049/jimmunol.1002302 21209287
47. Parseghian MH, Luhrs KA (2006) Beyond the walls of the nucleus: the role of histones in cellular signaling and innate immunity. Biochem Cell Biol 84: 589–604. doi: 10.1139/o06-082 16936831
48. Esquenet M, Swinnen JV, Heyns W, Verhoeven G (1997) LNCaP prostatic adenocarcinoma cells derived from low and high passage numbers display divergent responses not only to androgens but also to retinoids. J Steroid Biochem Mol Biol 62: 391–399. doi: 10.1016/S0960-0760(97)00054-X 9449242
49. Behrens I, Kissel T (2003) Do cell culture conditions influence the carrier-mediated transport of peptides in Caco-2 cell monolayers? Eur J Pharm Sci 19: 433–442. doi: 10.1016/S0928-0987(03)00146-5 12907294
50. Wenger SL, Senft JR, Sargent LM, Bamezai R, Bairwa N, et al. (2004) Comparison of established cell lines at different passages by karyotype and comparative genomic hybridization. Biosci Rep 24: 631–639. doi: 10.1007/s10540-005-2797-5 16158200
51. Martin B, Brenneman R, Becker KG, Gucek M, Cole RN, et al. (2008) iTRAQ analysis of complex proteome alterations in 3xTgAD Alzheimer′s mice: understanding the interface between physiology and disease. PLoS One 3: e2750. doi: 10.1371/journal.pone.0002750 18648646
52. Garver LS, Dong Y, Dimopoulos G (2009) Caspar controls resistance to Plasmodium falciparum in diverse anopheline species. PLoS Pathog 5: e1000335. doi: 10.1371/journal.ppat.1000335 19282971
53. Rodrigues J, Brayner FA, Alves LC, Dixit R, Barillas-Mury C (2010) Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science 329: 1353–1355. doi: 10.1126/science.1190689 20829487
54. Drevets DA, Campbell PA (1991) Macrophage phagocytosis: use of fluorescence microscopy to distinguish between extracellular and intracellular bacteria. J Immunol Methods 142: 31–38. doi: 10.1016/0022-1759(91)90289-R 1919019
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2015 Číslo 2
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Control of Murine Cytomegalovirus Infection by γδ T Cells
- ATPaseTb2, a Unique Membrane-bound FoF1-ATPase Component, Is Essential in Bloodstream and Dyskinetoplastic Trypanosomes
- Rational Development of an Attenuated Recombinant Cyprinid Herpesvirus 3 Vaccine Using Prokaryotic Mutagenesis and In Vivo Bioluminescent Imaging
- Direct Binding of Retromer to Human Papillomavirus Type 16 Minor Capsid Protein L2 Mediates Endosome Exit during Viral Infection