Nanoparticles and microparticles of polymers and polysaccharides to administer fish vaccines

Biological Research

Volumn 46, Issue 4, 2013, Pages 407-419

  Rivas Aravena, Andrea ^a   Sandino, Ana María ^a   Spencer, Eugenio ^a  

^a UNIVERSIDAD DE SANTIAGO DE CHILE   (Chile)

Author keywords

Aquaculture; Nanoparticles; Vaccine

Indexed keywords

ANTIGEN; NANOPARTICLE; POLYMER; POLYSACCHARIDE; VACCINE;

ANIMAL; AQUACULTURE; BIOTECHNOLOGY; FISH DISEASES; IMMUNOLOGY;

ANIMALS; ANTIGENS; AQUACULTURE; BIOTECHNOLOGY; FISH DISEASES; NANOPARTICLES; POLYMERS; POLYSACCHARIDES; VACCINES;

EID: 84893481270     PISSN: 07169760     EISSN: 07176287     Source Type: Journal    
DOI: 10.4067/S0716-97602013000400012     Document Type: Review

References (175)

1. ADOMAKO M, ST-HILAIRE S, ZHENG Y, ELEY J, MARCUM RD, SEALEY W, DONAHOWER BC, LAPATRA S, SHERIDAN PP (2012) Oral DNA vaccination of rainbow trout, Oncorhynchus mykiss (Walbaum), against infectious haematopoietic necrosis virus using PLGA [Poly(D,L-Lactic-Co-Glycolic Acid)] nanoparticles. J Fish Dis 35(3):203-214.
2. AGNIHOTRI SA, MALLIKARJUNA NN, AMINABHAVI TM (2004) Recent advances on chitosan-based micro-and nanoparticles in drug delivery. J Control Release 100(1):5-28.
3. ALTUN S, KUBILAY A, EKICI S, DIDINEN BI, DILER Ö (2010) Oral Vaccination Against Lactococcosis in Rainbow Trout (Oncorhynchus mykiss) Using Sodium Alginate and Poly (lactide-co-glycolide) Carrier. Journal of the Faculty of Veterinary Medicine, University of Kafkas, Kars 16:211-217.
4. ALTUN S, KUBILAY A, EKICI S, DIDINEN BI, DILER Ö (2010) Oral vaccination against Lactococcosis in Rainbow Trout (Oncorhynchusmykiss) Using Sodium Alginate and Poly (lactide-co-glycolide) carrier. Kafkas Univ Vet Fak Derg 16:211-217.
5. AUDRAN R, PETER K, DANNULL J, MEN Y, SCANDELLA E, GROETTRUP M, GANDER B, CORRADIN G (2003) Encapsulation of peptides in biodegradable microspheres prolongs their MHC class-I presentation by dendritic cells and macrophages in vitro. Vaccine 21(11-12):1250-1255.
6. BANCHEREAU J, STEINMAN RM (1998) Dendritic cell and the control of immunity. Nature 392(6673):245-252.
7. BANCHEREAU J, ZURAWSKI S, Thompson-Snipes L, BLANCK JP, CLAYTON S, MUNK A, CAO Y, WANG Z, KHANDELWAL S, HU J, MCCOY WHT, PALUCKA KA, REITER Y, FREMONT DH, ZURAWSKI G, COLONNA M, SHAW AS, KLECHEVSKY E (2012) Immunoglobulin like transcript receptors on human dermal CD14+ dendritic cells act as a CD8-antagonist to control cytotoxic T cell priming. Proc Natl Acad Sci U S A 109(46):18885-18890.
8. BASSITY E, CLARK TG (2012) Functional identification of dendritic cells in the teleost model, rainbow trout (Oncorhynchus mykiss). PLoS One 7(3):e33196.
9. BEHERA T, NANDA PK, MOHANTY C, MOHAPATRA D, SWAIN P, DAS BK, ROUTRAY P, MISHRA BK, SAHOO SK (2010) Parenteral immunization of fish, Labeo rohita with Poly D, L-lactide-co-glycolic acid (PLGA) encapsulated antigen microparticles promotes innate and adaptive immune responses. Fish Shellfish Immunol 28(2):320-325.
10. BERG A, RODSETH OM, TANGERAS A, HANSEN T (2006) Time of vaccination influences development of adhesions, growth and spinal deformities in Atlantic salmon Salmo salar. Diseases of aquatic organisms 69(2-3):239-248.
11. BORGES O, SILVA M, DE SOUSA A, BORCHARD G, JUNGINGER HE, Cordeiro-Da-Silva A (2008) Alginate coated chitosan nanoparticles are an effective subcutaneous adjuvant for hepatitis B surface antigen. International immunopharmacology 8(13-14):1773-1780.
12. BOUDINOT P, BLANCO M, DE KINKELIN P, BENMANSOUR A (1998) Combined DNA immunization with the glycoprotein gene of viral hemorrhagic septicemia virus and infectious hematopoietic necrosis virus induces double-specific protective immunity and nonspecific response in rainbow trout. Virology 249(2):297-306.
13. BOWERSOCK TL, HOGENESCH H, SUCKOW M, GUIMOND P, MARTIN S, BORIE D, TORREGROSA S, PARK H, PARK K (1999) Oral vaccination of animals with antigens encapsulated in alginate microspheres. Vaccine 17(13-14):1804-1811.
14. BRODE S, MACARY PA (2004) Cross-presentation: dendritic cells and macrophages bite off more than they can chew! Immunology 112(3):345-351.
15. BROOS S, LUNDBERG K, AKAGI T, KADOWAKI K, AKASHI M, GREIFF L, BORREBAECK CA, LINDSTEDT M (2010) Immunomodulatory nanoparticles as adjuvants and allergen-delivery system to human dendritic cells: Implications for specific immunotherapy. Vaccine 28(31):5075-5085.
16. BURGDORF S, KURTS C (2008) Endocytosis mechanisms and the cell biology of antigen presentation. Curr Opin Immunol 20(1):89-95.
17. CARRINGTON AC, SECOMBES CJ (2007) CpG oligodeoxynucleotides up-regulate antibacterial systems and induce protection against bacterial challenge in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 23(4):781-792.
18. CLAWSON C, HUANG CT, FUTALAN D, SEIBLE DM, SAENZ R, LARSSON M, MA W, MINEV B, ZHANG F, OZKAN M, OZKAN C, ESENER S, MESSMER D (2010) Delivery of a peptide via poly(D,L-lactic-co-glycolic) acid nanoparticles enhances its dendritic cell stimulatory capacity. Nanomedicine 6(5):651-661.
19. COESHOTT CM, SMITHSON SL, VERDERBER E, SAMANIEGO A, BLONDER JM, ROSENTHAL GJ, WESTERINK MA (2004) Pluronicm F127-based systemic vaccine delivery systems. Vaccine 22(19):2396-2405.
20. CORBEIL S, KURATH G, LAPATRA SE (2000) Fish DNA vaccine against infectious hematopoietic necrosis virus: efficacy of various routes of immunisation. Fish Shellfish Immunol 10(8):711-723.
21. CRUZ LJ, TACKEN PJ, FOKKINK R, FIGDOR CG (2011) The influence of PEG chain length and targeting moiety on antibody-mediated delivery of nanoparticle vaccines to human dendritic cells. Biomaterials 32(28):6791-6803.
22. CUESTA A, Chaves-Pozo E, De Las Heras Ai, Saint-Jean SR, Perez-Prieto S, TAFALLA C (2010) An active DNA vaccine against infectious pancreatic necrosis virus (IPNV) with a different mode of action than fish rhabdovirus DNA vaccines. Vaccine 28(19):3291-3300.
23. CHENG AC, CHEN YY, CHEN JC (2008) Dietary administration of sodium alginate and kappa-carrageenan enhances the innate immune response of brown-marbled grouper Epinephelus fuscoguttatus and its resistance against Vibrio alginolyticus. Vet Immunol Immunopathol 121(3-4):206-215.
24. CHONG CS, CAO M, WONG WW, FISCHER KP, ADDISON WR, KWON GS, TYRRELL DL, SAMUEL J (2005) Enhancement of T helper type 1 immune responses against hepatitis B virus core antigen by PLGA nanoparticle vaccine delivery. J Control Release 102(1):85-99.
25. DANHIER F, ANSORENA E, SILVA JM, COCO R, LE BRETON A, PREAT V (2012) PLGA-based nanoparticles: an overview of biomedical applications. J Control Release 161(2):505-522.
26. DAVIS SS (2006) The use of soluble polymers and polymer microparticles to provide improved vaccine responses after parenteral and mucosal delivery. Vaccine 24 Suppl 2:S2-7-10.
27. DE LAS HERAS AI, RODRÍGUEZ Saint-Jean S, Pérez-Prieto SI (2010) Immunogenic and protective effects of an oral DNA vaccine against infectious pancreatic necrosis virus in fish. Fish Shellfish Immunol 28(4):562-570.
28. DESAI MP, LABHASETWAR V, AMIDON GL, LEVY RJ (1996) Gastrointestinal uptake of biodegradable microparticles: effect of particle size. Pharm Res 13(12):1838-1845.
29. DESAI MP, LABHASETWAR V, WALTER E, LEVY RJ, AMIDON GL (1997) The mechanism of uptake of biodegradable microparticles in Caco-2 cells is size dependent. Pharm Res 14(11):1568-1573
30. DIWAN M, ELAMANCHILI P, CAO M, SAMUEL J (2004) Dose sparing of CpG oligodeoxynucleotide vaccine adjuvants by nanoparticle delivery. Curr Drug Deliv 1(4):405-412.
31. DIWAN M, ELAMANCHILI P, LANE H, GAINER A, SAMUEL J (2003) Biodegradable nanoparticle mediated antigen delivery to human cord blood derived dendritic cells for induction of primary T cell responses. J Drug Target 11(8-10):495-507.
32. DOGGETT TA, HARRIS JE (1991) Morphology of the gut associated lymphoid tissue of Oreochromis mossambicus and its role in antigen absorption. Fish & Shellfish Immunology 1:213-227.
33. DORSON M, CASTRIC J, TORCHY C (1978) Infectious pancreatic necrosis virus of salmonids: biological and antigenic features of a pathogenic strain and of a non-pathogenic variant selected in RTG-2 cells. J Fish Dis 1(4):309-320.
34. DOSHI N, PRABHAKARPANDIAN B, Rea-Ramsey A, PANT K, SUNDARAM S, MITRAGOTRI S (2010) Flow and adhesion of drug carriers in blood vessels depend on their shape: a study using model synthetic microvascular networks. J Control Release 146(2):196-200.
35. ELAMANCHILI P, DIWAN M, CAO M, SAMUEL J (2004) Characterization of poly(D,L-lactic-co-glycolic acid) based nanoparticulate system for enhanced delivery of antigens to dendritic cells. Vaccine 22(19):2406-2412.
36. ELAMANCHILI P, LUTSIAK CM, HAMDY S, DIWAN M, SAMUEL J (2007) "Pathogen-mimicking" nanoparticles for vaccine delivery to dendritic cells. J Immunother 30(4):378-395.
37. ELDAR A, HOROVITCZ A, BERCOVIER H (1997) Development and efficacy of a vaccine against Streptococcus iniae infection in farmed rainbow trout. Vet. Immunol. Immunopathol. 56:175-183.
38. ESPENES A, PRESS CM, ROOIJEN NV, LANDSVERK T (1997) Apoptosis in phagocytotic cells of lymphoid tissues in rainbow trout (Oncorhynchus mykiss) following administration of clodronate liposomes. Cell Tissue Res 289(2):323-331.
39. EVENSEN O, BRUDESETH B, MUTOLOKI S (2005) The vaccine formulation and its role in inflammatory processes in fish-effects and adverse effects. Developments in biologicals 121:117-125.
40. FEHR T, SKRASTINA D, PUMPENS P, ZINKERNAGEL RM (1998) T cell-independent type I antibody response against B cell epitopes expressed repetitively on recombinant virus particles. Proc Natl Acad Sci U S A 95(16):9477-9481.
41. Fernández-Alonso M, ÁLVAREZ F, ESTEPA A, BLASCO R, COLL JM (1999) A model to study fish DNA immersion vaccination by using the green fluorescent protein. Journal of Fish Diseases 22(3):237-241.
42. Fernández-Alonso M, ROCHA A, COLL JM (2001) DNA vaccination by immersion and ultrasound to trout viral haemorrhagic septicaemia virus. Vaccine 19(23-24):3067-3075.
43. FISCHER S, SCHLOSSER E, MUELLER M, CSABA N, MERKLE HP, GROETTRUP M, GANDER B (2009) Concomitant delivery of a CTL-restricted peptide antigen and CpG ODN by PLGA microparticles induces cellular immune response. J Drug Target 17(8):652-661
44. FOGED C, BRODIN B, FROKJAER S, SUNDBLAD A (2005) Particle size and surface charge affect particle uptake by human dendritic cells in an in vitro model. Int J Pharm 298(2):315-322.
45. FREDRIKSEN BN, GRIP J (2012) PLGA/PLA micro and nanoparticle formulations serve as antigen depots and induce elevated humoral responses after immunization of Atlantic salmon (Salmo salar L.). Vaccine 30(3):656-667.
46. FREDRIKSEN BN, SAEVAREID K, MCAULEY L, LANE ME, BOGWALD J, DALMO RA (2011) Early immune responses in Atlantic salmon (Salmo salar L.) after immunization with PLGA nanoparticles loaded with a model antigen and beta-glucan. Vaccine 29(46):8338-8349.
47. FUJIKI K, MATSUYAMAS H, YANO T (1994) Protective effect of sodium alginates against bacterial infection in common Carp, Cyprinus carpio L. J Fish Dis 17:349-355.
48. GARINOT M, FIEVEZ V, POURCELLE V, STOFFELBACH F, DES RIEUX A, PLAPIED L, THEATE I, FREICHELS H, JEROME C, Marchand-Brynaert J, SCHNEIDER YJ, PREAT V (2007) PEGylated PLGA-based nanoparticles targeting M cells for oral vaccination. J Control Release 120(3):195-204.
49. GEORGOPOULOU U, VERNIER JM (1986) Local immunological response in the posterior intestinal segment of the rainbow trout after oral administration of macromolecules. Developmental and comparative immunology 10(4):529-537.
50. GHENDON Y, MARKUSHIN S, KRIVTSOV G, AKOPOVA I (2008) Chitosan as an adjuvant for parenterally administered inactivated influenza vaccines. Archives of virology 153(5):831-837.
51. GLOMSKI CA, TAMBURLIN J, CHAINANI M (1992) The phylogenetic odyssey of the erythrocyte. III. Fish, the lower vertebrate experience. Histology and histopathology 7(3):501-528.
52. GOFORTH R, SALEM AK, ZHU X, MILES S, ZHANG XQ, LEE JH, SANDLER AD (2009) Immune stimulatory antigen loaded particles combined with depletion of regulatory T-cells induce potent tumor specific immunity in a mouse model of melanoma. Cancer Immunol Immunother 58(4):517-530.
53. Gómez-Casado E, ESTEPA A, COLL JM (2011) A comparative review on European-farmed finfish RNA viruses and their vaccines. Vaccine 29(15):2657-2671.
54. Gómez-Chiarri M, LIVINGSTON SK, Muro-Cacho C, SANDERS S, LEVINE RP (1996) Introduction of foreign genes into the tissue of live fish by direct injection and particle bombardment. Dis. aquat. Organisms 27(1):5-12.
55. GREGODIARIS G (1990) Immunotogicai adyuvants: a role for liposomes. Immunol Today 11:89-97.
56. GREGORIADIS G, BACON A, Caparros-Wanderley W, MCCORMACK B (2002) A role for liposomes in genetic vaccination. Vaccine 20 Suppl 5:B1-.
57. GUPTA RK, ALROY J, ALONSO MJ, LANGER R, SIBER GR (1997) Chronic local tissue reactions, long-term immunogenicity and immunologic priming of mice and guinea pigs to tetanus toxoid encapsulated in biodegradable polymer microspheres composed of poly lactide-coglycolide polymers. Vaccine 15(16):1716-1723.
58. GUTIERRO I, HERNÁNDEZ RM, IGARTUA M, GASCON AR, PEDRAZ JL (2002) Size dependent immune response after subcutaneous, oral and intranasal administration of BSA loaded nanospheres. Vaccine 21(1-2):67-77.
59. HAMDY S, HADDADI A, HUNG RW, LAVASANIFAR A (2011) Targeting dendritic cells with nano-particulate PLGA cancer vaccine formulations. Adv Drug Deliv Rev 63(10-11):943-955.
60. HAMDY S, HADDADI A, SOMAYAJI V, RUAN D, SAMUEL J (2007) Pharmaceutical analysis of synthetic lipid A-based vaccine adjuvants in poly (D,L-lactic-co-glycolic acid) nanoparticle formulations. J Pharm Biomed Anal 44(4):914-923.
61. HARDING CV, SONG R (1994) Phagocytic processing of exogenous particulate antigens by macrophages for presentation by class I MHC molecules. J Immunol 153(11):4925-4933.
62. HARIKRISHNAN R, BALASUNDARAM C, HEO MS (2012) Poly D,L-lactide-co-glycolic acid-liposome encapsulated ODN on innate immunity in Epinephelus bruneus against Vibrio alginolyticus. Vet Immunol Immunopathol 147(1-2):77-85.
63. HARIKRISHNAN R, BALASUNDARAM C, HEO MS (2012) Poly D,L-lactide-co-glycolic acid (PLGA)-encapsulated vaccine on immune system in Epinephelus bruneus against Uronema marinum. Experimental parasitology 131(3):325-332.
64. HASTEIN T, GUDDING R, EVENSEN O (2005) Bacterial vaccines for fish-an update of the current situation worldwide. Developments in biologicals 121:55-74.
65. HAUGLAND GT, JORDAL AE, WERGELAND HI (2012) Characterization of small, mononuclear blood cells from salmon having high phagocytic capacity and ability to differentiate into dendritic like cells. PLoS One 7(11):e49260.
66. HE C, HU Y, YIN L, TANG C, YIN C (2010) Effects of particle size and surface charge on cellular uptake and biodistribution of polymeric nanoparticles. Biomaterials 31(13):3657-3666.
67. HE X, JIANG L, WANG F, XIAO Z, LI J, LIU LS, LI D, REN D, JIN X, LI K, HE Y, SHI K, GUO Y, ZHANG Y, SUN S (2005) Augmented humoral and cellular immune responses to hepatitis B DNA vaccine adsorbed onto cationic microparticles. J Control Release 107(2):357-372.
68. HUTTENHUIS HB, RIBEIRO AS, BOWDEN TJ, VAN BAVEL C, TAVERNE.,THIELE AJ, ROMBOUT JH (2006) The effect of oral immuno-stimulation in juvenile carp (Cyprinus carpio L.). Fish Shellfish Immunol 21(3):261-271.
69. JOFFRÉ OP, SEGURA E, SAVINA A, AMIGORENA S (2012) Cross presentation by dendritic cells. Nat Rev Immunol 12(8):557-569.
70. JOHANSEN P, CORRADIN G, MERKLE HP, GANDER B (1998) Release of tetanus toxoid from adjuvants and PLGA microspheres: how experimental set-up and surface adsorption fool the pattern. J Control Release 56(1-3):209-217.
71. JOOSTEN PHM, TIEMERSMA E, THREELS A, Caumartin-Dhieux C, ROMBOUT Jhwm (1997) Oral vaccination of fish against Vibrio anguillarum using alginate microparticles. Fish & Shellfish Immunology 7:471-485.
72. KANELLOS TS, SYLVESTER ID, BUTLER VL, AMBALI AG, PARTIDOS CD, HAMBLIN AS, RUSSELL PH (1999) Mammalian granulocyte-macrophage colony-stimulating factor and some CpG motifs have an effect on the immunogenicity of DNA and subunit vaccines in fish. Immunology 96(4):507-510.
73. KATARE YK, MUTHUKUMARAN T, PANDA AK (2005) Influence of particle size, antigen load, dose and additional adjuvant on the immune response from antigen loaded PLA microparticles. Int J Pharm 301(1-2):149-160.
74. KATARE YK, PANDA AK (2006) Immunogenicity and lower dose requirement of polymer entrapped tetanus toxoid co-administered with alum. Vaccine 24(17):3599-3608.
75. KIM CH, JOHNSON MC, DRENNAN JD, SIMON BE, THOMANN E, LEONG JA (2000) DNA vaccines encoding viral glycoproteins induce nonspecific immunity and Mx protein synthesis in fish. J Virol 74(15):7048-7054.
76. KOELLNER B, KOTTERBA G (2002) Temperature dependent activation of leucocyte populations of rainbow trout, Oncorhynchus mykiss, after intraperitoneal immunisation with Aeromonas salmonicida. Fish & Shellfish Immunology 12:35-48.
77. KOPPANG EO, BJERKAS I, HAUGARVOLL E, CHAN EK, SZABO NJ, ONO N, AKIKUSA B, JIRILLO E, POPPE TT, SVEIER H, TORUD B, SATOH M (2008) Vaccination-induced systemic autoimmunity in farmed Atlantic salmon. J Immunol 181(7):4807-4814.
78. KOPPANG EO, HAUGARVOLL E, HORDVIK I, AUNE L, POPPE TT (2005) Vaccine-associated granulomatous inflammation and melanin accumulation in Atlantic salmon, Salmo salar L., white muscle. J Fish Dis 28(1):13-22.
79. KOPPOLU B, ZAHAROFF DA (2013) The effect of antigen encapsulation in chitosan particles on uptake, activation and presentation by antigen presenting cells. Biomaterials 34(9):2359-2369.
80. KOVEN W, BARR Y, HADAS E, Ben-Atia I, CHEN Y, WEISS R, TANDLER A (1999) The potential of liposomes as a nutrient supplement in frst-feeding marine sh larvae. Aquaculture Nutrition 5:251-256.
81. LAPATRA SE, CORBEIL S, JONES GR, SHEWMAKER WD, LORENZEN N, ANDERSON ED, KURATH G (2001) Protection of rainbow trout against infectious hematopoietic necrosis virus four days after specific or semi-specific DNA vaccination. Vaccine 19(28-29):4011-4019.
82. LAVELLE EC, JENKINS PG, HARRIS JE (1997) Oral immunization of rainbow trout with antigen microencapsulated in poly(DL-lactide-co-glycolide) microparticles. Vaccine. 15(10):1070-1078.
83. LEAL C, Carvalho-Castro G, SACCHETIN P, LOPES C, MORAES A, FIGUEIREDO HCP (2010) Oral and parenteral vaccines against Flavobacterium columnare: evaluation of humoral immune response by ELISA and in vivo efficiency in Nile tilapia (Oreochromis niloticus). Aquaculture International, 18(4):657-666(610).
84. LEE CH, JEONG HD, CHUNG JK, LEE HH, KIM KH (2003) CpG motif in synthetic ODN primes respiratory burst of olive flounder Paralichthys olivaceus phagocytes and enhances protection against Edwardsiella tarda. Diseases of aquatic organisms 56(1):43-48.
85. LEMOINE D, WAUTERS F, Bouchend'Homme S, PRÉAT V (1998) Preparation and characterization of alginate microspheres containing a model antigen. International Journal of Pharmaceutics 176(1): 9-19.
86. LI J, BARREDA DR, ZHANG YA, BOSHRA H, GELMAN AE, LAPATRA S, TORT L, SUNYER JO (2006) B lymphocytes from early vertebrates have potent phagocytic and microbicidal abilities. Nature immunology 7(10):1116-1124.
87. LI X, XU Y, CHEN G, WEI P, PING Q (2008) PLGA nanoparticles for the oral delivery of 5-Fluorouracil using high pressure homogenization-emulsification as the preparation method and in vitro/in vivo studies. Drug Dev Ind Pharm 34(1):107-115.
88. LILLEHAUG A (1989) Oral immunization of rainbow trout, Salmo gairdneri Richardson, against vibriosis with vaccines protected against digestive degradation. Journal of Fish Diseases 12:579-584.
89. LIM F, SUN AM (1980) Microencapsulated islets as bioartificial endocrine pancreas. Science 210(4472):908-910.
90. LORENZEN N, LORENZEN E, Einer-Jensen K, LAPATRA SE (2002) Immunity induced shortly after DNA vaccination of rainbow trout against rhabdoviruses protects against heterologous virus but not against bacterial pathogens. Developmental and comparative immunology 26(2):173-179.
91. LU JM, WANG X, Marin-Muller C, WANG H, LIN PH, YAO Q, CHEN C (2009) Current advances in research and clinical applications of PLGA-based nanotechnology. Expert Rev Mol Diagn 9(4):325-341.
92. Lugo-Villarino G, BALLA KM, STACHURA DL, BANUELOS K, WERNECK MB, TRAVER D (2010) Identification of dendritic antigen-presenting cells in the zebrafish. Proc Natl Acad Sci U S A 107(36):15850-15855.
93. LUMSDEN JS, FERGUSON HW (1994) Isolation and partial characterization of rainbow trout (Oncorhynchus mykiss) gill mucin. Fish Physiol. Biochem. 12(5):387-398.
94. LUTSIAK ME, ROBINSON DR, COESTER C, KWON GS, SAMUEL J (2002) Analysis of poly(D,L-lactic-co-glycolic acid) nanosphere uptake by human dendritic cells and macrophages in vitro. Pharm Res 19(10):1480-1487.
95. MA Y, ZHAO X, LI J, SHEN Q (2012) The comparison of different daidzein PLGA nanoparticles in increasing its oral bioavailability. Int J Nanomedicine 7:559-570.
96. MAKADIA HK, SIEGEL SJ (2011) Poly Lactic-co-Glycolic Acid (PLGA) as Biodegradable Controlled Drug Delivery Carrier. Polymers (Basel) 3(3):1377-1397.
97. MANOLOVA V, FLACE A, BAUER M, SCHWARZ K, SAUDAN P, BACHMANN MF (2008) Nanoparticles target distinct dendritic cell populations according to their size. Eur J Immunol 38(5):1404-1413.
98. Martínez-Alonso S, Martinez-Lopez A, ESTEPA A, CUESTA A, TAFALLA C (2011) The introduction of multi-copy CpG motifs into an antiviral DNA vaccine strongly up-regulates its immunogenicity in fish. Vaccine 29(6):1289-1296.
99. MAURICE S, NUSSINOVITCH A, JAFFE N, SHOSEYOV O, GERTLER A (2004) Oral immunization of Carassius auratus with modified recombinant A-layer proteins entrapped in alginate beads. Vaccine 23(4):450-459.
100. MBOW ML, DE GREGORIO E, VALIANTE NM, RAPPUOLI R (2010) New adjuvants for human vaccines. Curr Opin Immunol 22(3):411-416.
101. MENG Z, SHAO J, XIANG L (2003) CpG oligodeoxynucleotides activate grass carp (Ctenopharyngodon idellus) macrophages. Developmental and comparative immunology 27(4):313-321.
102. MESHKINI S, TAFY A-A, TUKMECHI A, Farhang-Pajuh F (2012) Effects of chitosan on hematological parameters and stress resistance in rainbow trout (Oncorhynchus mykiss). Veterinary Research Forum. 3(1):49-54.
103. MIDTLYNG PJ (1997) Vaccinated fish welfare: protection versus side-effects. Dev Biol Stand 90:371-379.
104. MORACHIS JM, MAHMOUD EA, ALMUTAIRI A (2012) Physical and chemical strategies for therapeutic delivery by using polymeric nanoparticles. Pharmacol Rev 64(3):505-519.
105. Munang'andu HM, FREDRIKSEN BN, MUTOLOKI S, BRUDESETH B, KUO TY, MARJARA IS, DALMO RA, EVENSEN O (2012) Comparison of vaccine efficacy for different antigen delivery systems for infectious pancreatic necrosis virus vaccines in Atlantic salmon (Salmo salar L.) in a cohabitation challenge model. Vaccine 30(27):4007-4016.
106. NAGAMOTO T, HATTORI Y, TAKAYAMA K, MAITANI Y (2004) Novel chitosan particles and chitosan-coated emulsions inducing immune response via intranasal vaccine delivery. Pharm Res 21(4):671-674.
107. NAHA PC, KANCHAN V, MANNA PK, PANDA AK (2008) Improved bioavailability of orally delivered insulin using Eudragit-L30D coated PLGA microparticles. J Microencapsul 25(4):248-256.
108. NAKATANI M, IWASAKI T, WATARAI S, KODAMA H (2007) In vitro enhancement by CpG ODN of phagocytic activity of rainbow trout head kidney phagocytes against fish pathogen Vibrio ordalii, but not against polystyrene particles. J Vet Med Sci 69(12):1287-1290
109. NAKHLA AN, SZALAI AJ, BANOUB JH, KEOUGH KMW (1994) Uptake and biodistribution of free and liposomally incorporated lipopolysaccharide of Aeromonas salmonicida administered via different routes to rainbow trout (Oncorhynchus mykiss). Journal of Liposome Research. 4:1029-11048.
110. NAKHLA AN, SZALAI AJ, BANOUB JH, KEOUGH KMW (1997) Serum anti-LPS antibody production by rainbow trout (Oncorhynchus mykiss) in response to the administration of free and liposomally-incorporated LPS from Aeromonas salmonicida. Fish & Shellfish Immunology 7:387-401.
111. NISHIMURA K, NISHIMURA S, NISHI N, SAIKI I, TOKURA S, AZUMA I (1984) Immunological activity of chitin and its derivatives. Vaccine 2(1):93-99.
112. NORTON LW, PARK J, BABENSEE JE (2010) Biomaterial adjuvant effect is attenuated by anti-inflammatory drug delivery or material selection. J Control Release 146(3):341-348.
113. O'DONNELL GB, REILLY P, DAVIDSON GA, ELLIS AE (1996) The uptake of human gamma globulin incorporated into poly (D,L-lactide-co-glycolide) microparticles following oral intubation in Atlantic salmon, Salmo salar L. Fish & Shellfish Immunology. 6:507-520.
114. OUJI Y, Yoshida-Terakura A, HAYASHI Y, MAEDA I, KAWASE M, YAMATO E, MIYAZAKI J, YAGI K (2002) Polyethyleneimine/chitosan hexamer-mediated gene transfection into intestinal epithelial cell cultured in serum-containing medium. J Biosci Bioeng 94(1):81-83.
115. OWENS DE, 3rd, PEPPAS NA (2006) Opsonization, biodistribution, and pharmacokinetics of polymeric nanoparticles. Int J Pharm 307(1):93-102.
116. PANDEY R, KHULLER GK (2007) Nanoparticle-based oral drug delivery system for an injectable antibiotic-streptomycin. Evaluation in a murine tuberculosis model. Chemotherapy 53(6):437-441.
117. PANYAM J, ZHOU WZ, PRABHA S, SAHOO SK, LABHASETWAR V (2002) Rapid endo-lysosomal escape of poly(DL-lactide-co-glycolide) nanoparticles: implications for drug and gene delivery. FASEB J 16(10):1217-1226.
118. PARRA D, RIEGER AM, LI J, ZHANG YA, RANDALL LM, HUNTER CA, BARREDA DR, SUNYER JO (2012) Pivotal advance: peritoneal cavity B-1 B cells have phagocytic and microbicidal capacities and present phagocytosed antigen to CD4+ T cells. Journal of leukocyte biology 91(4):525-536.
119. PELUSO G, PETILLO O, RANIERI M, SANTIN M, AMBROSIO L, CALABRO D, AVALLONE B, BALSAMO G (1994) Chitosan-mediated stimulation of macrophage function. Biomaterials 15(15):1215-1220.
120. PETTERSEN EF, INGERSLEV HC, STAVANG V, EGENBERG M, WERGELAND HI (2008) A highly phagocytic cell line TO from Atlantic salmon is CD83 positive and M-CSFR negative, indicating a dendritic like cell type. Fish Shellfish Immunol 25(6):809-819.
121. POLK AE, AMSDEN B, SCARRATT DJ, GONZAL A, OKHAMAFE AO, GOOSEN MFA (1994) Oral delivery in aquaculture: Controlled release of proteins from chitosan-alginate microcapsules. Aquacultural Engineering. 13(4):311-323.
122. POOLEY JL, HEATH WR, SHORTMAN K (2001) Cutting edge: intravenous soluble antigen is presented to CD4 T cells by CD8 dendritic cells, but cross-presented to CD8 T cells by CD8+ dendritic cells. J Immunol 166(9):5327-5330.
123. POPPE TT, BRECK. O (1997) Pathology of Atlantic salmon Salmo salar intraperitoneally immunized with oil-adjuvanted vaccine: a case report. Dis Aquat Org. 29:219-226.
124. PORPORATTO C, BIANCO ID, CORREA SG (2005) Local and systemic activity of the polysaccharide chitosan at lymphoid tissues after oral administration. Journal of leukocyte biology 78(1):62-69.
125. POWER CA, MARKHAM RJF, DONALD AW (1990) Uptake and tissue distribution of liposomes after intraperitoneal administration to rainbow trout, Oncorhynchus mykiss (Richardson): a preliminary report. Journal of Fish Diseases. 13:329-332.
126. PRIDGEON JW, KLESIUS PH, MU X, YANCEY RJ, KIEVIT MS, DOMINOWSKI PJ (2012) Efficacy of QCDCR formulated CpG ODN 2007 in Nile tilapia against Streptococcus iniae and identification of upregulated genes. Vet Immunol Immunopathol 145(1-2):179-190.
127. PROKOP A, DAVIDSON JM (2008) Nanovehicular intracellular delivery systems. J Pharm Sci 97(9):3518-3590.
128. QUENTEL C, VIGNEULLE M (1997) Antigen uptake and immune responses after oral vaccination. Dev Biol Stand 90:69-78.
129. RAJESH KUMAR S, ISHAQ AHMED VP, PARAMESWARAN V, SUDHAKARAN R, SARATH BABU V, SAHUL HAMEED AS (2008) Potential use of chitosan nanoparticles for oral delivery of DNA vaccine in Asian sea bass (Lates calcarifer) to protect from Vibrio (Listonella) anguillarum. Fish Shellfish Immunol 25(1-2):47-56.
130. RAMOS EA, RELUCIO JL, Torres-Villanueva CA (2005) Gene expression in tilapia following oral delivery of chitosan-encapsulated plasmid DNA incorporated into fish feeds. Marine biotechnology 7(2):89-94.
131. REDDY ST, REHOR A, SCHMOEKEL HG, HUBBELL JA, SWARTZ MA (2006) In vivo targeting of dendritic cells in lymph nodes with poly(propylene sulfide) nanoparticles. J Control Release 112(1):26-34.
132. RODGERS CJ (1990) Immersion vaccination for control of fish furunculosis. Dis Aquat Org. 8:69-72.
133. RODRIGUES AP, HIRSCH D, FIGUEIREDO HCP, LOGATO PVR, MORAES AM (2006) Production and characterisation of alginate microparticles incorporating Aeromonas hydrophila designed for fish oral vaccination. Process Biochem 41:638-643.
134. RODRÍGUEZ-PINTO D (2005) B cells as antigen presenting cells. Cell Immunol 238(2):67-75
135. ROMALDE JL, Luzardo-Álvarez A, RAVELO C, TORANZO AE, Blanco-Mendez J (2004) Oral immunization using alginate microparticles as a useful strategy for booster vaccination against fish lactococcosis. Aquaculture 236:119-129.
136. ROMALDE JL, MARGARIÑOS B, TORANZO AE (1999) Prevention of streptococcosis in turbot by intraperitoneal vaccination:a review. J. Appl. Ichthyol 15:153-158.
137. ROMBOUT JHWM, BERG AA, BERG CTGA, WITTE P, EGBERTS E (2006) mmunological importance of the second gut segment in carp. III. Systemic and/or mucosal immune responses after immunization with soluble or particulate antigen. Journal of Fish Biology 35(2):79-186.
138. ROMBOUT JHWM, VAN DEN BERG AA, VAN DER BERG CTGA, WITTE P, EGBERTS E (1989) Immunological importance of the second gut segment of carp. III. Systemic and/or mucosal immune responses after immunization with soluble or particulate antigen. Journal of Fish Biology 35:179-186.
139. ROMOREN K, THU BJ, SMISTAD G, EVENSEN O (2002) Immersion delivery of plasmid DNA. I. A study of the potentials of a liposomal delivery system in rainbow trout (Oncorhynchus mykiss) fry. J Control Release 85(1-3):203-213.
140. Salgado-Miranda C, Loza-Rubio E, Rojas-Anaya E, GARCÍA.,ESPINOSA G (2013) Viral vaccines for bony fish: past, present and future. Expert review of vaccines 12(5):567-578.
141. SALINAS I, ZHANG YA, SUNYER JO (2011) Mucosal immunoglobulins and B cells of teleost fish. Developmental and comparative immunology 35(12):1346-1365.
142. SCHLOSSER E, MUELLER M, FISCHER S, BASTA S, BUSCH DH, GANDER B, GROETTRUP M (2008) TLR ligands and antigen need to be coencapsulated into the same biodegradable microsphere for the generation of potent cytotoxic T lymphocyte responses. Vaccine 26(13):1626-1637.
143. SHAIKH J, ANKOLA DD, BENIWAL V, SINGH D, KUMAR MN (2009) Nanoparticle encapsulation improves oral bioavailability of curcumin by at least 9-fold when compared to curcumin administered with piperine as absorption enhancer. Eur J Pharm Sci 37(3-4):223-230.
144. SHEN H, ACKERMAN AL, CODY V, GIODINI A, HINSON ER, CRESSWELL P, EDELSON RL, SALTZMAN WM, HANLON DJ (2006) Enhanced and prolonged cross-presentation following endosomal escape of exogenous antigens encapsulated in biodegradable nanoparticles. Immunology 117(1):78-88.
145. SIGAL LJ, CROTTY S, ANDINO R, ROCK KL (1999) Cytotoxic T-cell immunity to virus-infected non-haematopoietic cells requires presentation of exogenous antigen. Nature 398(6722):77-80.
146. SINGH M, SRIVASTAVA I (2003) Advances in vaccine adjuvants for infectious diseases. Current HIV research 1(3):309-320.
147. SKJERMO J, BERGHB Ø (2004) High-M alginate immunostimulation of Atlantic halibut (Hippoglossus hippoglossus L.) larvae using Artemia for delivery, increases resistance against vibriosis. Aquaculture 238(1-4):107-113.
148. SKJERMO J, DEFOORT T, DEHASQUE M, ESPEVIK T, OLSEN Y, SKJAK BRAEK G, SORGELOOS P, VADSTEIN O (1995) Immunostimulation of juvenile turbot Scophthalmus maximus L. using an alginate with high mannuronic acid content administered via the live food organism Artemia. Fish and Shellfish Immunology 5(7): 531-534.
149. SOMMERSET I, KROSSOY B, BIERING E, FROST P (2005) Vaccines for fish in aquaculture. Expert review of vaccines 4(1):89-101.
150. SUDHA P, S. L, KWANG J, GONG Z (2001) Multiple tissue transformation in adult zebrafish by gene gun bombardment and muscular injection of naked DNA Mar Biotechnol (NY). 3(2):19-25.
151. SZELEI J, VARADI L, MULLER F, ERDIELYI F, ORBAN L, HORVATH L, DUDA E (1994) Liposome-mediated gene transfer in fish embryos. Transgenic Research. 3:116-119.
152. TAFAGHODI M, TABASI S, PAYANA M (2007) Alginate Microsphere as a Delivery System and Adjuvant for Autoclaved Leishmania major and Quillaja Saponin: Preparation and Characterization. Iranian Journal of Pharmaceutical Sciences 3(2):61-68.
153. TAMBER H, JOHANSEN P, MERKLE HP, GANDER B (2005) Formulation aspects of biodegradable polymeric microspheres for antigen delivery. Adv Drug Deliv Rev 57(3):357-376.
154. TANAKA H, MATSUMURA M, VELIKY IA (1984) Diffusion characteristics of substrates in Ca-alginate gel beads. Biotech. Bioeng. 26:53-58.
155. TASSAKKA A, SAKAI M (2003) The in vitro effect of CpG-ODNs on the innate immune response of common carp, Cyprinus carpio L. Aquaculture 220:27-36.
156. TASSAKKA A, SAKAI M (2004) Expression of immune-related genes in the common carp (Cyprinus carpio L.) after stimulation by CpG oligodeoxynucleotides. Aquaculture 242:1-12.
157. THIELE L, Rothen-Rutishauser B, JILEK S, Wunderli-Allenspach H, MERKLE HP, WALTER E (2001) Evaluation of particle uptake in human blood monocyte-derived cells in vitro. Does phagocytosis activity of dendritic cells measure up with macrophages? J Control Release 76(1-2):59-71.
158. TIAN J, SUN X, CHEN X, YU J, QU L, WANG L (2008) The formulation and immunisation of oral poly(DL-lactide-co-glycolide) microcapsules containing a plasmid vaccine against lymphocystis disease virus in Japanese flounder (Paralichthys olivaceus). International immunopharmacology 8(6):900-908.
159. TIAN J, YU J (2011) Poly(lactic-co-glycolic acid) nanoparticles as candidate DNA vaccine carrier for oral immunization of Japanese flounder (Paralichthys olivaceus) against lymphocystis disease virus. Fish Shellfish Immunol 30(1):109-117.
160. TIAN J, YU J, SUN X (2008) Chitosan microspheres as candidate plasmid vaccine carrier for oral immunisation of Japanese flounder (Paralichthys olivaceus). Vet Immunol Immunopathol 126(3-4):220-229.
161. TIAN JY, SUN XQ, CHEN XG (2008) Formation and oral administration of alginate microspheres loaded with pDNA coding for lymphocystis disease virus (LCDV) to Japanese flounder. Fish Shellfish Immunol 24(5):592-599.
162. TOYOKAWA H, NAKAO A, BAILEY RJ, NALESNIK MA, KAIZU T, LEMOINE JL, IKEDA A, TOMIYAMA K, PAPWORTH GD, HUANG L, DEMETRIS AJ, STARZL TE, MURASE N (2008) Relative contribution of direct and indirect allorecognition in developing tolerance after liver transplantation. Liver transplantation: official publication of the American Association for the Study of Liver Diseases and the International Liver Transplantation Society 14(3):346-357.
163. TYAGI RK, GARG NK, SAHU T (2012) Vaccination Strategies against Malaria: novel carrier(s) more than a tour de force. J Control Release 162(1):242-254.
164. VALLEJO AN, MILLER NW, HARVEY NE, CUCHENS MA, WARR GW, CLEM LW (1992) Cellular pathway(s) of antigen processing and presentation in fish APC: endosomal involvement and cell-free antigen presentation. Dev Immunol 3(1):51-65.
165. VERT M, MAUDUIT J, LI S (1994) Biodegradation of PLA/GA polymers: increasing complexity. Biomaterials 15(15):1209-1213.
166. WALDEN P, NAGY ZA, KLEIN J (1986) Major histocompatibility complex-restricted and unrestricted activation of helper T cell lines by liposome-bound antigens. The Journal of molecular and cellular immunology: JMCI 2(4):191-197.
167. WALSH MC, BANAS JA, MUDZINSKI SP, PREISSLER MT, GRAZIANO RF, GOSSELIN EJ (2003) A two-component modular approach for enhancing T-cell activation utilizing a unique anti-FcgammaRI-streptavidin construct and microspheres coated with biotinylated-antigen. Biomolecular engineering 20(1):21-33.
168. WANG G, PAN L, ZHANG Y (2011) Approaches to improved targeting of DNA vaccines. Human vaccines 7(12):1271-1281.
169. WANG XM, RUAN Y, XIE QD, HUANG TH (2005) Research on gene transfer by spermatozoa. Yi chuan = Hereditas/Zhongguo yi chuan xue hui bian ji 27(2):195-200.
170. WEE S, GOMBOTZ WR (1998) Protein release from alginate matrices. Adv Drug Deliv Rev 31(3):267-285.
171. WETZEL SA, PARKER DC (2006) MHC transfer from APC to T cells following antigen recognition. Crit Rev Immunol 26(1):1-21.
172. WONG G, KAATTARI, S L. & CHRISTENSEN J.M. (1992) Effectiveness of an oral enteric coated Vibrio vaccine for use in salmonid fish. Immunological Investigations 21:353-364.
173. YEH SP, CHANG CA, CHANG CY, LIU CH, CHENG W (2008) Dietary sodium alginate administration affects fingerling growth and resistance to Streptococcus sp. and iridovirus, and juvenile non-specific immune responses of the orange-spotted grouper, Epinephelus coioides. Fish Shellfish Immunol 25(1-2):19-27.
174. ZAHAROFF DA, ROGERS CJ, HANCE KW, SCHLOM J, GREINER JW (2007) Chitosan solution enhances both humoral and cell-mediated immune responses to subcutaneous vaccination. Vaccine 25(11):2085-2094.
175. ZHENG FR, SUN XQ, LIU HZ, ZHANG JX (2006) Study on the distribution and expression of a DNA vaccine against lymphocystis disease virus in Japanese flounder (Paralichthys olivaceus). Aquaculture 261(4):1128-1134.