Parental Transfer of the Antimicrobial Protein LBP/BPI Protects Eggs against Oomycete Infections

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Vertebrate females transfer antibodies via the placenta, colostrum and milk or via the egg yolk to protect their immunologically immature offspring against pathogens. This evolutionarily important transfer of immunity is poorly documented in invertebrates and basic questions remain regarding the nature and extent of parental protection of offspring. In this study, we show that a lipopolysaccharide binding protein/bactericidal permeability increasing protein family member from the invertebrate Biomphalaria glabrata (BgLBP/BPI1) is massively loaded into the eggs of this freshwater snail. Native and recombinant proteins displayed conserved LPS-binding, antibacterial and membrane permeabilizing activities. A broad screening of various pathogens revealed a previously unknown biocidal activity of the protein against pathogenic water molds (oomycetes), which is conserved in human BPI. RNAi-dependent silencing of LBP/BPI in the parent snails resulted in a significant reduction of reproductive success and extensive death of eggs through oomycete infections. This work provides the first functional evidence that a LBP/BPI is involved in the parental immune protection of invertebrate offspring and reveals a novel and conserved biocidal activity for LBP/BPI family members.

Vyšlo v časopise: Parental Transfer of the Antimicrobial Protein LBP/BPI Protects Eggs against Oomycete Infections. PLoS Pathog 9(12): e32767. doi:10.1371/journal.ppat.1003792
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1003792

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Zdroje

1. FlajnikMF, Du PasquierL (2004) Evolution of innate and adaptive immunity: can we draw a line? Trends Immunol 25: 640–644.

2. HasselquistD, NilssonJA (2009) Maternal transfer of antibodies in vertebrates: trans-generational effects on offspring immunity. Philos Trans R Soc Lond B Biol Sci 364: 51–60.

3. ChucriTM, MonteiroJM, LimaAR, SalvadoriML, KfouryJRJr, et al. (2010) A review of immune transfer by the placenta. J Reprod Immunol 87: 14–20.

4. SwainP, NayakSK (2009) Role of maternally derived immunity in fish. Fish Shellfish Immunol 27: 89–99.

5. HaineER (2008) Symbiont-mediated protection. Proc Biol Sci 275: 353–361.

6. JaenikeJ, UncklessR, CockburnSN, BoelioLM, PerlmanSJ (2010) Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science 329: 212–215.

7. HoffmannJA, ReichhartJM (2002) Drosophila innate immunity: an evolutionary perspective. Nat Immunol 3: 121–126.

8. DishawLJ, LitmanGW (2009) Invertebrate allorecognition: the origins of histocompatibility. Curr Biol 19: R286–288.

9. MarquisCP, BairdAH, de NysR, HolmströmC, KoziumiN (2005) An evaluation of the antimicrobial properties of the eggs of 11 species of scleractinian corals. Coral Reefs 24: 248–253.

10. LiangY, ZhangS, WangZ (2009) Alternative complement activity in the egg cytosol of amphioxus Branchiostoma belcheri: evidence for the defense role of maternal complement components. PLoS One 4: e4234.

11. FrauneS, AugustinR, BoschTC (2011) Embryo protection in contemporary immunology: Why bacteria matter. Commun Integr Biol 4: 369–372.

12. Groombridge B, Jenkins MD (2002) World Atlas of Biodiversity: earth's living resources in the 21st century: University of California Press, Berkeley, USA. 360 p.

13. GryseelsB, PolmanK, ClerinxJ, KestensL (2006) Human schistosomiasis. Lancet 368: 1106–1118.

14. PimentelD (1957) Life History of Australorbis glabratus, The Intermediate Snail Host of Schistosoma mansoni in Puerto Rico. Ecology 38: 576–580.

15. HathawayJJ, AdemaCM, StoutBA, MobarakCD, LokerES (2010) Identification of protein components of egg masses indicates parental investment in immunoprotection of offspring by Biomphalaria glabrata (gastropoda, mollusca). Dev Comp Immunol 34: 425–435.

16. BingleCD, CravenCJ (2004) Meet the relatives: a family of BPI- and LBP-related proteins. Trends Immunol 25: 53–55.

17. BeamerLJ, FischerD, EisenbergD (1998a) Detecting distant relatives of mammalian LPS-binding and lipid transport proteins. Protein Sci 7: 1643–1646.

18. CannyG, LevyO (2008) Bactericidal/permeability-increasing protein (BPI) and BPI homologs at mucosal sites. Trends Immunol 29: 541–547.

19. ElsbachP, WeissJ (1993) The bactericidal/permeability-increasing protein (BPI), a potent element in host-defense against gram-negative bacteria and lipopolysaccharide. Immunobiology 187: 417–429.

20. FentonMJ, GolenbockDT (1998) LPS-binding proteins and receptors. J Leukoc Biol 64: 25–32.

21. ElsbachP, WeissJ (1998) Role of the bactericidal/permeability-increasing protein in host defence. Curr Opin Immunol 10: 45–49.

22. SchultzH, HumeJ, Zhang deS, GioanniniTL, WeissJP (2007) A novel role for the bactericidal/permeability increasing protein in interactions of gram-negative bacterial outer membrane blebs with dendritic cells. J Immunol 179: 2477–2484.

23. WeissJ (2003) Bactericidal/permeability-increasing protein (BPI) and lipopolysaccharide-binding protein (LBP): structure, function and regulation in host defence against Gram-negative bacteria. Biochem Soc Trans 31: 785–790.

24. MarraMN, WildeCG, CollinsMS, SnableJL, ThorntonMB, et al. (1992) The role of bactericidal/permeability-increasing protein as a natural inhibitor of bacterial endotoxin. J Immunol 148: 532–537.

25. SchumannRR, LeongSR, FlaggsGW, GrayPW, WrightSD, et al. (1990) Structure and function of lipopolysaccharide binding protein. Science 249: 1429–1431.

26. AltincicekB, VilcinskasA (2007) Analysis of the immune-related transcriptome of a lophotrochozoan model, the marine annelid Platynereis dumerilii. Front Zool 4: 18.

27. GonzalezM, GueguenY, Destoumieux-GarzonD, RomestandB, FievetJ, et al. (2007) Evidence of a bactericidal permeability increasing protein in an invertebrate, the Crassostrea gigas Cg-BPI. Proc Natl Acad Sci U S A 104: 17759–17764.

28. KrasityBC, TrollJV, WeissJP, McFall-NgaiMJ (2011) LBP/BPI proteins and their relatives: conservation over evolution and roles in mutualism. Biochem Soc Trans 39: 1039–1044.

29. GuillouF, MittaG, GalinierR, CoustauC (2007) Identification and expression of gene transcripts generated during an anti-parasitic response in Biomphalaria glabrata. Dev Comp Immunol 31: 657–671.

30. de Jong-Brink M, Goldschmeding J (1983) Endocrine and nervous regulation of female reproductive activity in the gonad and albumen gland of Lymnaea stagnalis. In: Lever JB, HH., editor. Molluscan Neuroendocrinology. Amsterdam: North Holland Press pp. 126–131.

31. MillerAN, OforiK, LewisF, KnightM (1996) Schistosoma mansoni: use of a subtractive cloning strategy to search for RFLPs in parasite-resistant Biomphalaria glabrata. Exp Parasitol 84: 420–428.

32. BeamerLJ, CarrollSF, EisenbergD (1998b) The BPI/LBP family of proteins: a structural analysis of conserved regions. Protein Sci 7: 906–914.

33. TanNS, HoB, DingJL (2000) High-affinity LPS binding domain(s) in recombinant factor C of a horseshoe crab neutralizes LPS-induced lethality. FASEB J 14: 859–870.

34. CapodiciC, ChenS, SidorczykZ, ElsbachP, WeissJ (1994) Effect of lipopolysaccharide (LPS) chain length on interactions of bactericidal/permeability-increasing protein and its bioactive 23-kilodalton NH2-terminal fragment with isolated LPS and intact Proteus mirabilis and Escherichia coli. Infect Immun 62: 259–265.

35. Gazzano-SantoroH, ParentJB, GrinnaL, HorwitzA, ParsonsT, et al. (1992) High-affinity binding of the bactericidal/permeability-increasing protein and a recombinant amino-terminal fragment to the lipid A region of lipopolysaccharide. Infect Immun 60: 4754–4761.

36. LampingN, HoessA, YuB, ParkTC, KirschningCJ, et al. (1996) Effects of site-directed mutagenesis of basic residues (Arg 94, Lys 95, Lys 99) of lipopolysaccharide (LPS)-binding protein on binding and transfer of LPS and subsequent immune cell activation. J Immunol 157: 4648–4656.

37. KamounS (2003) Molecular genetics of pathogenic oomycetes. Eukaryot Cell 2: 191–199.

38. PhillipsAJ, AndersonVL, RobertsonEJ, SecombesCJ, van WestP (2008) New insights into animal pathogenic oomycetes. Trends Microbiol 16: 13–19.

39. BalakrishnanA, MaratheSA, JoglekarM, ChakravorttyD (2012) Bactericidal/permeability increasing protein: A multifaceted protein with functions beyond LPS neutralization. Innate Immun 19(4): 339–47.

40. GalianaE, FourreS, EnglerG (2008) Phytophthora parasitica biofilm formation: installation and organization of microcolonies on the surface of a host plant. Environ Microbiol 10: 2164–2171.

41. BaiG, LiJ, ChristensenBM, YoshinoTP (1996) Phenoloxidase activity in the reproductive system and egg masses of the pulmonate gastropod, Biomphalaria glabrata. Comp Biochem Physiol B Biochem Mol Biol 114: 353–359.

42. BenkendorffK, DavisAR, BremnerJB (2001) Chemical defense in the egg masses of benthic invertebrates: an assessment of antibacterial activity in 39 mollusks and 4 polychaetes. J Invertebr Pathol 78: 109–118.

43. MukaiST, HoqueT, MorishitaF, SaleuddinASM (2004) Cloning and Characterization of a Candidate Nutritive Glycoprotein from the Albumen Gland of the Freshwater Snail, Helisoma duryi (Mollusca: Pulmonata). Invertebrate Biology 123: 83–92.

44. TakamatsuN, ShibaT, MuramotoK, KamiyaH (1995) Molecular cloning of the defense factor in the albumen gland of the sea hare Aplysia kurodai. FEBS Lett 377: 373–376.

45. SanchezJF, LescarJ, ChazaletV, AudfrayA, GagnonJ, et al. (2006) Biochemical and structural analysis of Helix pomatia agglutinin. A hexameric lectin with a novel fold. J Biol Chem 281: 20171–20180.

46. WeissJ, Beckerdite-QuagliataS, ElsbachP (1980) Resistance of gram-negative bacteria to purified bactericidal leukocyte proteins: relation to binding and bacterial lipopolysaccharide structure. J Clin Invest 65: 619–628.

47. SchroderNW, SchumannRR (2005) Non-LPS targets and actions of LPS binding protein (LBP). J Endotoxin Res 11: 237–242.

48. ZweignerJ, GrammHJ, SingerOC, WegscheiderK, SchumannRR (2001) High concentrations of lipopolysaccharide-binding protein in serum of patients with severe sepsis or septic shock inhibit the lipopolysaccharide response in human monocytes. Blood 98: 3800–3808.

49. BeakesGW, GlocklingSL, SekimotoS (2012) The evolutionary phylogeny of the oomycete “fungi”. Protoplasma 249: 3–19.

50. van WestP (2006) Saprolegnia parasitica, an oomycete pathogen with a fishy appetite: new challenges for an old problem. Mycologist 20: 99–104.

51. RomansicJM, DiezKA, HigashiEM, JohnsonJE, BlausteinAR (2009) Effects of the pathogenic water mold Saprolegnia ferax on survival of amphibian larvae. Dis Aquat Organ 83: 187–193.

52. JudelsonHS (2012) Dynamics and innovations within oomycete genomes: insights into biology, pathology, and evolution. Eukaryot Cell 11: 1304–1312.

53. Baron O, Reichhart JM, Ponchet M, Coustau C (2013) Anti-oomycete activity fo lipopolysaccharide (LPS)-binding proteins/bactericidal/permeability-increasing proteins. WO/2013/120619. In: INRA/CNRS, editor. WIPO Patentscope. France.

54. TylerBM (2009) Entering and breaking: virulence effector proteins of oomycete plant pathogens. Cell Microbiol 11: 13–20.

55. MelidaH, Sandoval-SierraJV, Dieguez-UribeondoJ, BuloneV (2013) Analyses of extracellular carbohydrates in oomycetes unveil the existence of three different cell wall types. Eukaryot Cell 12: 194–203.

56. AltschulSF, MaddenTL, SchafferAA, ZhangJ, ZhangZ, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389–3402.

57. LarkinMA, BlackshieldsG, BrownNP, ChennaR, McGettiganPA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947–2948.

58. SchultzJ, CopleyRR, DoerksT, PontingCP, BorkP (2000) SMART: a web-based tool for the study of genetically mobile domains. Nucleic Acids Res 28: 231–234.

59. NielsenH, KroghA (1998) Prediction of signal peptides and signal anchors by a hidden Markov model. Proc Int Conf Intell Syst Mol Biol 6: 122–130.

60. GuillouF, MittaG, DissousC, PierceR, CoustauC (2004) Use of individual polymorphism to validate potential functional markers: case of a candidate lectin (BgSel) differentially expressed in susceptible and resistant strains of Biomphalaria glabrata. Comp Biochem Physiol B Biochem Mol Biol 138: 175–181.

61. LimmerS, HallerS, DrenkardE, LeeJ, YuS, et al. (2011) Pseudomonas aeruginosa RhlR is required to neutralize the cellular immune response in a Drosophila melanogaster oral infection model. Proc Natl Acad Sci U S A 108: 17378–17383.

62. Baeza GarciaA, PierceRJ, GourbalB, WerkmeisterE, ColinetD, et al. (2010) Involvement of the cytokine MIF in the snail host immune response to the parasite Schistosoma mansoni. PLoS Pathog 6: e1001115.

63. van WestP, de BruijnI, MinorKL, PhillipsAJ, RobertsonEJ, et al. (2010) The putative RxLR effector protein SpHtp1 from the fish pathogenic oomycete Saprolegnia parasitica is translocated into fish cells. FEMS Microbiol Lett 310: 127–137.

64. MittaG, GalinierR, TisseyreP, AllienneJF, Girerd-ChambazY, et al. (2005) Gene discovery and expression analysis of immune-relevant genes from Biomphalaria glabrata hemocytes. Dev Comp Immunol 29: 393–407.

65. TauszigS, JouanguyE, HoffmannJA, ImlerJ-L (2000) Toll-related receptors and the control of antimicrobial peptide expression in Drosophila. Proceedings of the National Academy of Sciences 97: 10520–10525.

66. GardsvollH, HansenLV, JorgensenTJ, PlougM (2007) A new tagging system for production of recombinant proteins in Drosophila S2 cells using the third domain of the urokinase receptor. Protein Expr Purif 52: 384–394.

67. BerneyM, HammesF, BosshardF, WeilenmannHU, EgliT (2007) Assessment and interpretation of bacterial viability by using the LIVE/DEAD BacLight Kit in combination with flow cytometry. Appl Environ Microbiol 73: 3283–3290.

68. HetruC, BuletP (1997) Strategies for the isolation and characterization of antimicrobial peptides of invertebrates. Methods Mol Biol 78: 35–49.

69. BarbaultF, LandonC, GuenneuguesM, MeyerJP, SchottV, et al. (2003) Solution structure of Alo-3: a new knottin-type antifungal peptide from the insect Acrocinus longimanus. Biochemistry 42: 14434–14442.

70. HopeACA (1968) A Simplified Monte Carlo Significance Test Procedure. Journal of the Royal Statistical Society Series B (Methodological) 30: 582–598.

71. Team RDC (2005) R: A language and environment for statistical computing. In: Computing FfS, editor. 2.11.1 ed. Vienna, Austria.