Immune responses during the larval stages of Mytilus galloprovincialis: Metamorphosis alters immunocompetence, body shape and behavior

Fish and Shellfish Immunology

Volumn 35, Issue 2, 2013, Pages 438-447

  Balseiro, Pablo ^a   Moreira, Rebeca ^a   Chamorro, Rubén ^a   Figueras, Antonio ^a   Novoa, Beatriz ^a  

^a INSTITUTO DE INVESTIGACIONES MARINAS   (Spain)

Author keywords

Antimicrobial; Larvae; Metamorphosis; Mussel; Ontogeny

Indexed keywords

BACTERIA (MICROORGANISMS); BIVALVIA; ESCHERICHIA COLI; MYTILUS GALLOPROVINCIALIS;

EID: 84880043396     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2013.04.044     Document Type: Article

References (56)

1. Bishop C.D., Huggett M.J., Heyland A., Hodin J., Brandhorst B.P. Interspecific variation in metamorphic competence in marine invertebrates: the significance for comparative investigations into the timing of metamorphosis. Integr Comp Biol 2006, 46:662-682.
2. Halanych K.M. The new view of animal phylogeny. Annu Rev Ecol Evol Syst 2004, 35:229-256.
3. Eckman J.E. Closing the larval loop: linking larval ecology to the population dynamics of marine benthic invertebrates. JExp Mar Biol Ecol 1996, 200:207-237.
4. Lambert C., Nicolas J.L., Cilia V., Corre S. Vibrio pectenicida sp. nov., a pathogen of scallop (Pecten maximus) larvae. Int J Syst Bacteriol 1998, 48:481-487.
5. Shia A.K., Glittenberg M., Thompson G., Weber A.N., Reichhart J.M., Ligoxygakis P. Toll-dependent antimicrobial responses in Drosophila larval fat body require Spatzle secreted by haemocytes. JCell Sci 2009, 122:4505-4515.
6. Makki R., Meister M., Pennetier D., Ubeda J.-M., Braun A., Daburon V., et al. Ashort receptor downregulates JAK/STAT signalling to control the Drosophila cellular immune response. PLoS Biol 2010, 8:e1000441.
7. Ogawa A., Streit A., Antebi A., Sommer R.J. Aconserved endocrine mechanism controls the formation of Dauer and infective larvae in nematodes. Curr Biol 2009, 19:67-71.
8. Fisheries and aquaculture topics. The State of World Fisheries and Aquaculture (SOFIA). Topics fact sheets 2012, 150. FAO, FAO Fisheries and Aquaculture Department, Food and Agricultural Organization (FAO), Rome, Italy. J.-F. Pulvenis (Ed.).
9. Wootton E.C., Dyrynda E.A., Pipe R.K., Ratcliffe N.A. Comparisons of PAH-induced immunomodulation in three bivalve molluscs. Aquat Toxicol 2003, 65:13-25.
10. Morgan J.A.T., Dejong R.J., Snyder S.D., Mkogi G.M., Loker E.S. Schistosoma mansoni and Biomphalaria: past history and future trends. Parasitology 2001, 123:211-228.
11. Degnan S.M., Degnan B.M. The initiation of metamorphosis as an ancient polyphenic trait and its role in metazoan life-cycle evolution. Phil Trans R Soc B 2010, 365:641-651.
12. Williams E.A., Degnan S.M. Carry-over effect of larval settlement cue on postlarval gene expression in the marine gastropod Haliotis asinina. Mol Ecol 2009, 18:4434-4449.
13. Dyachuk V.A., Plotnikov S.V., Odintsova N.A. Appearance of muscle proteins in ontogenesis of the mussel Mytilus trossulus (Bivalvia). Russ J Mar Biol/Biol Morya 2005, 31:327-330.
14. Ellis I., Kempf S.C. Characterization of the central nervous system and various peripheral innervations during larval development of the oyster Crassostrea virginica. Invertebr Biol 2011, 130:236-250.
15. Jenny M.J., Warr G.W., Ringwood A.H., Baltzegar D.A., Chapman R.W. Regulation of metallothionein genes in the American oyster (Crassostrea virginica): ontogeny and differential expression in response to different stressors. Gene 2006, 379:156-165.
16. Tirapé A., Bacque C., Brizard R., Vandenbulcke F., Boulo V. Expression of immune-related genes in the oyster Crassostrea gigas during ontogenesis. Dev Comp Immunol 2007, 31:859-873.
17. Montagnani C., Tirape A., Boulo V., Escoubas J.M. The two Cg-timp mRNAs expressed in oyster hemocytes are generated by two gene families and differentially expressed during ontogenesis. Dev Comp Immunol 2005, 29:831-839.
18. Dyrynda E.A., Pipe R.K., Ratcliffe N.A. Host defence mechanisms in marine invertebrate larvae. Fish Shellfish Immunol 1995, 5:569-580.
19. Hadfield M.G., Carpizo-Ituarte E.J., del Carmen K., Nedved B.T. Metamorphic competence, a major adaptive convergence in marine invertebrate larvae. Am Zool 2001, 41:1123-1131.
20. Pawlik J.R. Chemical ecology of the settlement of benthic marine invertebrates. Oceanogr Mar Biol Annu Rev 1992, 30:273-335.
21. Degnan B.M., Morse D.E. Developmental and morphogenetic gene regulation in Haliotis rufescens larvae at metamorphosis. Am Zool 1995, 35:391-398.
22. Romero A., Dios S., Poisa-Beiro L., Costa M.M., Posada D., Figueras A., et al. Individual sequence variability and functional activities of fibrinogen-related proteins (FREPs) in the Mediterranean mussel (Mytilus galloprovincialis) suggest ancient and complex immune recognition models in invertebrates. Dev Comp Immunol 2011, 35:334-344.
23. Balseiro P., Falcó A., Romero A., Dios S., Martínez-López A., Figueras A., et al. Mytilus galloprovincialis myticin C: a chemotactic molecule with antiviral activity and immunoregulatory properties. PLoS ONE 2011, 6:e23140.
24. Pfaffl M.W. Anew mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29:e45.
25. Ruiz M., Tarifeno E., Llanos-Rivera A., Padget C., Campos B. Temperature effect in the embryonic and larval development of the mussel, Mytilus galloprovincialis (Lamarck, 1819). Rev Biol Mar Oceanogr 2008, 43:51-61.
26. Sánchez-Lazo C., Martínez-Pita I. Effect of temperature on survival, growth and development of Mytilus galloprovincialis larvae. Aquacult Res 2012, 43:1127-1133.
27. His E., Robert R., Dinet A. Combined effects of temperature and salinity on fed and starved larvae of the Mediterranean mussel Mytilus galloprovincialis and the Japanese oyster Crassostrea gigas. Mar Biol 1989, 100:455-463.
28. Satuito C.G., Natoyama K., Yamazaki M., Fusetani N. Larval development of the mussel Mytilus edulis galloprovincialis cultured under laboratory conditions. Fish Sci 1994, 60:65-68.
29. Elston R. Functional anatomy, histology and ultrastructure of the soft tissues of the larval American oyster, Crassostrea virginica. Proc Natl Shellfish Ass 1980, 70:65-93.
30. Elston R. Functional morphology of the coelomocytes of the larval oysters (Crassostrea virginica and Crassostrea gigas). JMar Biol Assoc UK 1980, 60:947-957.
31. Vernon P.J., Tang D. Eat-me: autophagy, phagocytosis, and reactive oxygen species signaling. Antioxid Redox Signal 2012.
32. Prado-Álvarez M., Romero A., Balseiro P., Dios S., Novoa B., Figueras A. Morphological characterization and functional immune response of the carpet shell clam (Ruditapes decussatus) haemocytes after bacterial stimulation. Fish Shellfish Immunol 2012, 32:69-78.
33. García-García E., Prado-Álvarez M., Novoa B., Figueras A., Rosales C. Immune responses of mussel hemocyte subpopulations are differentially regulated by enzymes of the PI 3-K, PKC, and ERK kinase families. Dev Comp Immunol 2008, 32:637-653.
34. Torreilles J., Guerin M.C., Roch P. Peroxidase-release associated with phagocytosis in Mytilus galloprovincialis haemocytes. Dev Comp Immunol 1997, 21:267-275.
35. Sardina J.L., López-Ruano G., Sánchez-Sánchez B., Llanillo M., Hernández-Hernández A. Reactive oxygen species: are they important for haematopoiesis?. Crit Rev Oncol/Hematol 2012, 81:257-274.
36. O'Brien J.J., Spinelli S.L., Tober J., Blumberg N., Francis C.W., Taubman M.B., et al. 15-deoxy-δ12,14-PGJ2 enhances platelet production from megakaryocytes. Blood 2008, 112:4051-4060.
37. Owusu-Ansah E., Banerjee U. Reactive oxygen species prime Drosophila haematopoietic progenitors for differentiation. Nature 2009, 461:537-541.
38. Kuzin B., Roberts I., Peunova N., Enikolopov G. Nitric oxide regulates cell proliferation during Drosophila development. Cell 1996, 87:639-649.
39. Enikolopov G., Banerji J., Kuzin B. Nitric oxide and Drosophila development. Cell Death Differ 1999, 6:956-963.
40. Hodin J. Expanding networks: signaling components in and a hypothesis for the evolution of metamorphosis. Integr Comp Biol 2006, 46:719-742.
41. Cheng T.C. Bivalves. Invertebrate blood cells 1981, 233-300. Academic Press, London. N.A. Ratcliffe, A.F. Rowley (Eds.).
42. Mitta G., Vandenbulcke F., Noel T., Romestand B., Beauvillain J.C., Salzet M., et al. Differential distribution and defence involvement of antimicrobial peptides in mussel. JCell Sci 2000, 113(Pt 15):2759-2769.
43. Estévez-Calvar N., Romero A., Figueras A., Novoa B. Involvement of pore-forming molecules in immune defense and development of the Mediterranean mussel (Mytilus galloprovincialis). Dev Comp Immunol 2011, 35:1017-1031.
44. Hathaway J.J.M., Adema C.M., Stout B.A., Mobarak C.D., Loker E.S. Identification of protein components of egg masses indicates parental investment in immunoprotection of offspring by Biomphalaria glabrata (Gastropoda, Mollusca). Dev Comp Immunol 2010, 34:425-435.
45. Jackson D., Leys S.P., Hinman V.F., Woods R., Lavin M.F., Degnan B.M. Ecological regulation of development: induction of marine invertebrate metamorphosis. Int J Dev Biol 2002, 46:679-686.
46. Hadfield M.G. Why and how marine-invertebrate larvae metamorphose so fast. Semin Cell Dev Biol 2000, 11:437-443.
47. Zhou Z., Wang L., Shi X., Yue F., Wang M., Zhang H., et al. The expression of dopa decarboxylase and dopamine beta hydroxylase and their responding to bacterial challenge during the ontogenesis of scallop Chlamys farreri. Fish Shellfish Immunol 2012, 33:67-74.
48. Ge H., Wang G., Zhang L., Zhang Z., Wang S., Zou Z., et al. Molecular cloning and expression of interleukin-1 receptor-associated kinase 4, an important mediator of toll-like receptor signal pathway, from small abalone Haliotis diversicolor. Fish Shellfish Immunol 2011, 30:1138-1146.
49. Davidson B., Swalla B.J. Amolecular analysis of ascidian metamorphosis reveals activation of an innate immune response. Development 2002, 129:4739-4751.
50. Andersen Ø., Torgersen J., Pagander H., Magnesen T., Johnston I. Gene expression analyses of essential catch factors in the smooth and striated adductor muscles of larval, juvenile and adult great scallop (Pecten maximus). JMuscle Res Cell Motil 2009, 30:233-242.
51. Fabioux C., Huvet A., Lelong C., Robert R., Pouvreau S., Daniel J.Y., et al. Oyster vasa-like gene as a marker of the germline cell development in Crassostrea gigas. Biochem Biophys Res Commun 2004, 320:592-598.
52. Wang X., Liu B., Xiang J. Cloning, characterization and expression of ferritin subunit from clam Meretrix meretrix in different larval stages. Comp Biochem Physiol B Biochem Mol Biol 2009, 154:12-16.
53. Rahman M.M., McFadden G. Modulation of NF-κB signalling by microbial pathogens. Nat Rev Micro 2011, 9:291-306.
54. Li H., Venier P., Prado-Álvarez M., Gestal C., Toubiana M., Quartesan R., et al. Expression of Mytilus immune genes in response to experimental challenges varied according to the site of collection. Fish Shellfish Immunol 2010, 28:640-648.
55. Costa M.M., Prado-Álvarez M., Gestal C., Li H., Roch P., Novoa B., et al. Functional and molecular immune response of Mediterranean mussel (Mytilus galloprovincialis) haemocytes against pathogen-associated molecular patterns and bacteria. Fish Shellfish Immunol 2009, 26:515-523.
56. Mitta G., Hubert F., Dyrynda E.A., Boudry P., Roch P. Mytilin B and MGD2, two antimicrobial peptides of marine mussels: gene structure and expression analysis. Dev Comp Immunol 2000, 24:381-393.