Proliferation and resistance difference of a liver-parasitized myxosporean in two different gynogenetic clones of gibel carp

Parasitology Research

Volumn 113, Issue 4, 2014, Pages 1331-1341

  Zhai, Yan Hua ^a   Zhou, Li ^a   Wang, Yang ^a   Wang, Zhong Wei ^a   Li, Zhi ^a   Zhang, Xiao Juan ^a   Gui, Jian Fang ^a  

^a INSTITUTE OF HYDROBIOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

POLYCLONAL ANTIBODY; PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CLONE; CONTROLLED STUDY; DISEASE RESISTANCE; FISH; GENETIC ANALYSIS; GIBEL CARP; IMMUNOFLUORESCENCE; LIVER; MYXOBOLUS; MYXOBOLUS WULII; MYXOZOA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

CYPRINIDAE; MYXOBOLUS; MYXOSPOREA;

ANIMALS; AQUACULTURE; BASE SEQUENCE; CARPS; DISEASE RESISTANCE; GENES, MHC CLASS I; LIVER; MOLECULAR SEQUENCE DATA; MYXOBOLUS;

EID: 84897021612     PISSN: 09320113     EISSN: 14321955     Source Type: Journal    
DOI: 10.1007/s00436-014-3772-5     Document Type: Article

References (58)

1. Biedzka-Sarek M, Metso J, Kateifides A, Meri T, Jokiranta TS, Muszyński A, Radziejewska-Lebrecht J, Zannis V, Skurnik M, Jauhiainen M (2011) Apolipoprotein A-I exerts bactericidal activity against Yersinia enterocolitica serotype O:3. J Biol Chem 286: 38211-38219
2. Canning EU, Okamura B (2003) Biodiversity and evolution of the Myxozoa. Adv Parasitol 56:43-131 (Pubitemid 37532271)
3. Chang MX, Nie P, Liu G, Song Y, Gao Q (2005) Identification of immune genes in grass carp Ctenopharyngodon idella in response to infection of the parasitic copepod Sinergasilus major. Parasitol Res 96:224-229 (Pubitemid 40933670)
4. Choudhury M, Yamada S, Komatsu M, Kishimura H, Ando S (2009) Homologue of mammalian apolipoprotein A-II in non-mammalian vertebrates. Acta Biochim Biophys Sin (Shanghai) 41:370-378
5. Concha MI, Molina S, Oyarzún C, Villanueva J, Amthauer R (2003) Local expression of apolipoprotein AI gene and a possible role for HDL in primary defence in the carp skin. Fish Shellfish Immun 14: 259-273 (Pubitemid 36339520)
6. Dan C, Mei J, Wang D, Gui JF (2013) Genetic differentiation and efficient sex-specific marker development of a pair of Y- and X-linked markers in yellow catfish. Int J Biol Sci 9(10):1043-1049
7. Dobson CB, Sales SD, Hoggard P, Wozniak MA, Crutcher KA (2006) The receptor-binding region of human apolipoprotein E has direct anti-infective activity. J Infect Dis 193:442-450 (Pubitemid 43122345)
8. Eizaguirre C, Lenz TL, Kalbe M, Milinski M (2012) Rapid and adaptive evolution of MHC genes under parasite selection in experimental vertebrate populations. Nat Commun 3:621
9. Forbes S, McBain AJ, Felton-Smith S, Jowitt TA, Birchenough HL, Dobson CB (2013) Comparative surface antimicrobial properties of synthetic biocides and novel human apolipoprotein E derived antimicrobial peptides. Biomaterials 34:5453-5464
10. Gui JF, Zhou L (2010) Genetic basis and breeding application of clonal diversity and dual reproduction modes in polyploid Carassius auratus gibelio. Sci China Life Sci 53:409-415
11. Gui JF, Zhu ZY (2012) Molecular basis and genetic improvement of economically important traits in aquaculture animals. Chin Sci Bull 57:1751-1760
12. GuoW, Gui JF (2008) Microsatellite marker isolation and cultured strain identification in Carassius auratus gibelio.Aquacult Int 16:497-510
13. Jiang FF, Wang ZW, Zhou L, Jiang L, Zhang XJ, Apalikova OV, Brykov VA, Gui JF (2013) High male incidence and evolutionary implications of triploid form in northeast Asia Carassius auratus complex. Mol Phylogenet Evol 66:350-359
14. Kelly B, Harrison I, McKnight Á, Dobson C (2010) Anti-infective activity of apolipoprotein domain derived peptides in vitro: identification of novel antimicrobial peptides related to apolipoprotein B with anti-HIVactivity. BMC Immunol 11:13
15. Kent ML, Andree KB, Bartholomew JL, El-Matbouli M, Desser SS, Devlin RH, Feist SW, Hedrick RP, Hoffmann RW, Khattra J, Hallett SL, Lester RJG, Longshaw M, Palenzeula O, Siddall ME, Xiao CX (2001) Recent advances in our knowledge of the Myxozoa. J Eukaryot Microbiol 48:395-413 (Pubitemid 32656691)
16. KlitzW, Hedrick P, Louis EJ (2012) New reservoirs of HLA alleles: pools of rare variants enhance immune defense. Trends Genet 8:480-486
17. Li FB, Gui JF (2008) Clonal diversity and genealogical relationships of gibel carp in four hatcheries. Anim Genet 39:28-33
18. Liao IC, Huang TS, Tsai WS, Hsueh CM, Chang SL, Leano EM (2004) Cobia culture in Taiwan: current status and problems. Aquaculture 237:155-165 (Pubitemid 38893804)
19. Liu Y, Gu ZM, Luo YL (2010) Some additional data to the occurrence, morphology and validity of Myxobolus turpisrotundus Zhang, 2009 (Myxozoa: Myxosporea). Parasitol Res 107:67-73
20. Liu Y, Whipps C, Gu ZM, Zeng LB, Huang MJ (2012) Myxobolus honghuensis n. sp. (Myxosporea: Bivalvulida) parasitizing the pharynx of allogynogenetic gibel carp Carassius auratus gibelio (Bloch) from Honghu Lake, China. Parasitol Res 110:1331-1336
21. Lom J, Dyková I (2006) Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol (Praha) 53:1-36
22. Lu Y, Li M, Wu Y, Wang J (2002) Antigenic study of Myxobolus rotundus (Myxozoa: Myxosporea) using monoclonal antibodies. J Fish Dis 25:307-310 (Pubitemid 34527465)
23. Lu YS, Nie P (2004) Phylogenetic analysis of the myxosporeans parasitic in freshwater fish of China based on 18 S ribosomal DNA (in Chinese with English surmmary). Acta Hydrobiol Sin 28:587-591
24. Markiw ME, Wolf K (1974) Myxosoma cerebralis: isolation and concentration from fish skeletal elements-sequential enzymatic digestions and purification by differential centrifugation. J Fish Res Board Can 31:15-20
25. Mei J, Yue HM, Li Z, Chen B, Zhong JX, Dan C, Zhou L, Gui JF (2014) C1q-like factor, a target of miR-430, regulates primordial germ cell development in early embryos of Carassius auratus. Int J Biol Sci 10(1):15-24
26. Molnár K, Cech G, Székely C (2011) Histological and molecular studies of species of Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea) in the gills of Abramis, Blicca and Vimba spp. (Cyprinidae), with the redescription of M. macrocapsularis Reuss, 1906 and M. bliccae Donec & Tozyyakova, 1984. Parasitol Res 79:109-121. doi:10.1007/s11230-011-9292-0
27. Morris D (2010) Cell formation by myxozoan species is not explained by dogma. P Roy Soc B-Biol Sci 277:2565-2570
28. Morris D (2012) A newmodel formyxosporean (Myxozoa) development explains the endogenous budding phenomenon, the nature of cell within cell life stages and evolution of parasitism from a cnidarian ancestor. Int J Parasitol 42:829-840
29. Morris D, Freeman MA (2010) Hyperparasitism has wide-ranging implications for studies on the invertebrate phase of myxosporean (Myxozoa) life cycles. Int J Parasitol 40:357-69
30. Oǧuz MC (1999) Cystic liver disease caused by Myxobolus sp. in goldfish (Carassius auratus). Tur J Biol 23:199-205
31. Peng JX, Xie JL, Zhou L, Hong YH, Gui JF (2009) Evolutionary conservation of Dazl genomic organization and its continuous and dynamic distribution throughout germline development in gynogenetic gibel carp. J Exp Zool Part B 312:855-871
32. Pereiro P, Balseiro P, Romero A, Dios S, Forn-Cuni G, Fuste B, Planas JV, Beltran S, Novoa B, Figueras A (2012) High-throughput sequence analysis of turbot (Scophthalmus maximus) transcriptome using 454-pyrosequencing for the discovery of antiviral immune genes. PLoS One 7:e35369
33. Rajan B, Lokesh J, Kiron V, Brinchmann MF (2013) Differentially expressed proteins in the skin mucus of Atlantic cod (Gadus morhua) upon natural infection with Vibrio anguillarum. BMC Vet Res 9:103
34. Rangel LF, Santos MJ, Cech G, Szekely C (2009) Morphology,molecular data, and development of Zschokkella mugilis (Myxosporea, Bivalvulida) in a polychaete alternate host, Nereis diversicolor. J Parasitol 95:561-569
35. Rossignol T, Kelly B, Dobson CB, d'Enfert C (2011) Endocytosis-mediated vacuolar accumulation of the human ApoE apolipoprotein-derived ApoEdpL-Wantimicrobial peptide contributes to its antifungal activity in Candida albicans. Antimicrob Agents Ch 55:4670-4681
36. Sarropoulou E, Sepulcre P, Poisa-Beiro L, Mulero V, Meseguer J, Figueras A, Novoa B, Terzoglou V, Reinhardt R, Magoulas A (2009) Profiling of infection specific mRNA transcripts of the European seabass Dicentrarchus labrax. BMC Genomics 10:157
37. Siddall M, Martin D, Bridge D, Desser S, Cone D (1995) The demise of a phylum of protists: phylogeny of Myxozoa and other parasitic cnidaria. J Parasitol 81:961-7 (Pubitemid 26012355)
38. Tenger C, Zhou X (2003) Apolipoprotein Emodulates immune activation by acting on the antigen-presenting cell. Immunol 109:392-397 (Pubitemid 36783265)
39. Thomopson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.Nucleic Acids Res 25:4882-4896
40. Villarroel F, Bastías A, Casado A, Amthauer R, Concha MI (2007) Apolipoprotein A-I, an antimicrobial protein in Oncorhynchus mykiss: evaluation of its expression in primary defence barriers and plasma levels in sick and healthy fish. Fish Shellfish Immun 23:197-209 (Pubitemid 46635177)
41. Wang ZW, Zhu HP, Wang D, Jiang FF, Guo W, Zhou L, Gui JF (2011) A novel nucleo-cytoplasmic hybrid clone formed via androgenesis in polyploid gibel carp. BMC Res Notes 4:82
42. Wang Y, Zhou L, Li Z, Li WH, Gui JF (2013) Apolipoprotein C1 regulates epiboly during gastrulation in zebrafish. Sci China Life Sci 56(11):975-984
43. Wu YS, Wang JG (1997) A new species of Myxosporidian from allogynogenetic silver crussian carp (Myxosporea: BibalvulidaI, Myxobolidae). Acta Hydrobiol Sin 21:268
44. Xia W, Zhou L, Yao B, Li CJ, Gui JF (2007) Differential and spermatogenic cell-specific expression of DMRT1 during sex reversal in protogynous hermaphroditic groupers. Mol Cell Endocrinol 263:156-172 (Pubitemid 44834554)
45. Xia JH, Liu JX, Zhou L, Li Z, Gui JF (2008) Apo-14 is required for digestive system organogenesis during fish embryogenesis and larval development. Int J Dev Biol 52:1089
46. Yang L, Gui JF (2004) Positive selection on multiple antique allelic lineages of transferrin in the polyploid Carassius auratus. Mol Biol Evol 21:1264-1277 (Pubitemid 38823729)
47. Ye LT, Li WX, Wu SG, Wang GT (2012) Supplementary studies on Henneguya doneci Schulman, 1962 (Myxozoa: Myxosporea) infecting the gill filaments of Carassius auratus gibelio (Bloch) in China: histologic, ultrastructural, and molecular data. Parasitol Res 110: 1509-1516. doi:10.1007/s00436-011-2655-2
48. Yokoyama H (2003) A review: gaps in our knowledge on myxozoan parasites of fishes. Fish Pathol 38:125-136
49. Yokoyama H, Ogawa K, Wakabayashi H (1992) Branchial pathology of cyprinid fish infected with myxosporean parasites. In: Shariff M, Subasinghe RP, Arthur JR (eds) Diseases in Asian aquaculture. Asian Fisheries Society, Manila, pp 337-343
50. Yokoyama H, Grabner D, Shirakashi S (2012) Transmission biology of the Myxozoa. In: Carvalho E, David GS, Silva RJ (eds) Health and environment in aquaculture. InTech, Rijeka, pp 3-42
51. Zhai Y, Zhou L, Jf G (2012) Identification and characterization of one novel type of Triactinospomyxon with short spore axis. Parasitol Res 110:2385-2393
52. Zhang JY, Wang JG, Li AH, Gong XN (2010a) Infection of Myxobolus turpisrotundus sp. n. in allogynogenetic gibel carp, Carassius auratus gibelio (Bloch), with revision of Myxobolus rotundus (sl) Nemeczek reported from C. auratus auratus (L.). J Fish Dis 33:625-638
53. Zhang JY, Yokoyama H, Wang JG, Li AH, Gong XN, Ryu-Hasegawa IM, Ogawa K (2010b) Utilization of tissue habitats by Myxobolus wulii Landsberg & Lom, 1991 in different carp hosts and disease resistance in allogynogenetic gibel carp: redescription of M. wulii from China and Japan. J Fish Dis 33:57-68
54. Zhao YJ, Li NN, Tang FH, Dong JL (2013) Remarks on the validity of Myxobolus ampullicapsulatus and Myxobolus honghuensis (Myxozoa: Myxosporea) based on SSU rDNA sequences. Parasitol Res 112:3817-3823. doi:10.1007/s00436- 013-3569-y
55. Zhou L, Gui JF (2002) Karyotypic diversity in polyploid gibel carp, Carassius auratus gibelio Bloch. Genetica 115:223-232 (Pubitemid 35181306)
56. Zhou L, Wang Y, Gui JF (2000) Genetic evidence for gonochoristic reproduction in gynogenetic silver crucian carp (Carassius auratus gibelio Bloch) as revealed by RAPD assays. J Mol Evol 51:498-506
57. Zhou L, Wang Y, Gui JF (2001) Molecular analysis of silver crucian carp (Carassius auratus gibelio Bloch) clones by SCAR markers. Aquaculture 201:219-228 (Pubitemid 32943704)
58. Zhu X, Parks JS (2012) New roles of HDL in inflammation and hematopoiesis. Annu Rev Nutr 32:161-182