Mucins as Diagnostic and Prognostic Biomarkers in a Fish-Parasite Model: Transcriptional and Functional Analysis

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Pérez Sánchez, Jaume ^a   Estensoro, Itziar ^a   Redondo, María José ^a   Calduch Giner, Josep Alvar ^a   Kaushik, Sadasivam ^b   Sitjà Bobadilla, Ariadna ^a  

^a CSIC Instituto de Acuicultura de Torre de la Sal IATS   (Spain)

^b UR1067 Nutrition Metabolism Aquaculture   (France)

Author keywords

[No Author keywords available]

Indexed keywords

FISH OIL; MUCIN; MUCIN 13; MUCIN 18; MUCIN 19; MUCIN 2; MUCIN 2 LIKE PROTEIN; RNA; TRANSCRIPTOME; UNCLASSIFIED DRUG; VEGETABLE OIL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENTEROMYXUM LEEI; ESOPHAGUS; FISH; GENE EXPRESSION; GENE SEQUENCE; GILL; GILTHEAD SEA BREAM; MYXOZOA; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITOSIS; PHYLOGENY; PROGNOSIS; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SCREENING; SEA BREAM; SKIN; STOMACH; TISSUE DISTRIBUTION; TRANSCRIPTION REGULATION;

ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; BASE SEQUENCE; BIOLOGICAL MARKERS; CLUSTER ANALYSIS; DATABASES, GENETIC; DNA PRIMERS; FISH OILS; GASTROINTESTINAL TRACT; GENE EXPRESSION REGULATION; GILLS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HOST-PARASITE INTERACTIONS; MOLECULAR SEQUENCE DATA; MUCINS; PHYLOGENY; PLANT OILS; REAL-TIME POLYMERASE CHAIN REACTION; SEA BREAM; SKIN;

ARCHOSARGUS RHOMBOIDALIS; ENTEROMYXUM LEEI; MAMMALIA;

EID: 84878919234     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065457     Document Type: Article

References (79)

1. Gendler SJ, Spicer AP, (1995) Epithelial mucin genes. Annu Rev Plant Physiol 57: 607-634.
2. Desseyn JL, Aubert JP, Porchet N, Laine A, (2000) Evolution of the large secreted gel-forming mucins. Mol Biol Evol 17: 1175-1184.
3. Moniaux N, Escande F, Porchet N, Aubert JP, Batra SK, (2001) Structural organization and classification of the human mucin genes. Front Biosci 6: D1192-D1206.
4. Desseyn JL, (2009) Mucin CYS domains are ancient and highly conserved modules that evolved in concert. Mol Phylogenet Evol 52: 284-292.
5. Duraisamy S, Ramasamy S, Kharbanda S, Kufe D, (2006) Distinct evolution of the human carcinoma-associated transmembrane mucins, MUC1, MUC4 and MUC16. Gene 373: 28-34.
6. Desseyn JL, Tetaert D, Gouyer V, (2008) Architecture of the large membrane-bound mucins. Gene 410: 215-222.
7. Desseyn JL, Clavereau I, Laine A, (2002) Cloning, chromosomal localization and characterization of the murine mucin gene orthologous to human MUC4. Eur J Biochem 269: 3150-3159.
8. Chaturvedi P, Singh AP, Batra SK, (2007) Structure, evolution, and biology of the MUC4 mucin. FASEB 22: 966-81.
9. Lang T, Hansson GC, Samuelsson T, (2007) Gel-forming mucins appeared early in metazoan evolution. PNAS 104: 16209-16214.
10. Sasaki M, Ikeda H, Nakanuma Y, (2007) Expression profiles of MUC mucins and trefoil factor family (TFF) peptides in the intrahepatic biliary system: Physiological distribution and pathological significance. Prog Histochem Cytochem 42: 61-110.
11. Carraway KL, Ramsauer VP, Haq B, Carraway CAC, (2003) Cell signaling through membrane mucins. BioEssays 25: 66-71.
12. Hollingsworth MA, Swanson BJ, (2004) Mucins in cancer: Protection and control of the cell surface. Nat Rev Cancer 4: 45-60.
13. Valque H, Gouyer V, Gottrand F, Desseyn JL, (2012) MUC5B leads to aggressive behavior of breast cancer MCF7 cells. PLoS ONE 7: e46699.
14. Kufe DW, (2009) Mucins in cancer: function, prognosis and therapy. Nat Rev Cancer 9: 874-885.
15. Calduch-Giner JA, Bermejo-Nogales A, Benedito-Palos L, Estensoro I, Ballester-Lozano G, et al. (2013) Deep sequencing for de novo construction of a marine fish (Sparus aurata) transcriptome database with a large coverage of protein-coding transcripts. BMC Genomics 14: 178.
16. Sitjà-Bobadilla A, Palenzuela O (2012) Enteromyxum species. In: Woo PTK, Buchmann K, editors. Fish Parasites: Pathobiology and Protection. CABI. 163-176.
17. Estensoro I, Benedito-Palos L, Palenzuela O, Kaushik S, Sitjà-Bobadilla A, et al. (2011) The nutritional background of the host alters the disease course in a fish-myxosporean system. Vet Parasitol 175: 141-150.
18. Calduch-Giner JA, Sitjà-Bobadilla A, Davey GC, Cairns MT, Kaushik S, et al. (2012) Dietary vegetable oils do not alter the intestine transcriptome of gilthead sea bream (Sparus aurata), but modulate the transcriptomic response to infection with Enteromyxum leei. BMC Genomics 13: 470.
19. Estensoro I, Redondo MJ, Salesa B, Kaushik S, Pérez-Sánchez J, et al. (2012) Effect of nutrition and Enteromyxum leei infection on gilthead sea bream Sparus aurata intestinal carbohydrate distribution. Dis Aquat Org 100: 29-42.
20. Estensoro I, Redondo MJ, Álvarez-Pellitero P, Sitjà-Bobadilla A, (2010) Novel horizontal transmission route for Enteromyxum leei (Myxozoa) by anal intubation of gilthead sea bream Sparus aurata. Dis Aquat Org 92: 51-58.
21. Calduch-Giner J, Mingarro M, de Celis SVR, Boujard D, Pérez-Sánchez J, (2003) Molecular cloning and characterization of gilthead sea bream, (Sparus aurata) growth hormone receptor (GHR). Assessment of alternative splicing. Comp Biochem Physiol B Biochem Mol Biol 136: 1-13.
22. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCr method. Methods 25: 402-408.
23. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
24. Sheng YH, Hasnain SZ, Florin THJ, McGuckin MA, (2012) Mucins in inflammatory bowel diseases and colorectal cancer. J Gastroenterol Hepatol 27: 28-38.
25. Mahomed F, (2011) Recent advances in mucin immunohistochemistry in salivary gland tumors and head and neck squamous cell carcinoma. Oral Oncol 47: 797-803.
26. Yonezawa S, Higashi M, Yamada N, Yokoyama S, Kitamoto S, et al. (2011) Mucins in human neoplasms: Clinical pathology, gene expression and diagnostic application. Pathol Int 61: 697-716.
27. Schroers V, Van der Marel M, Neuhaus H, Steinhagen D, (2009) Changes of intestinal mucus glycoproteins after peroral application of Aeromonas hydrophila to common carp (Cyprinus carpio). Aquaculture 288: 184-189.
28. Gheorghiu C, Marcogliese DJ, Scott ME, (2012) Waterborne zinc alters temporal dynamics of guppy Poecilia reticulata epidermal response to Gyrodactylus turnbulli (Monogenea). Dis Aquat Org 98: 143-153.
29. Estensoro I, Jung-Schroers V, Álvarez-Pellitero P, Steinhagen D, Sitjà-Bobadilla A, (2013) Effects of Enteromyxum leei (Myxozoa) infection on gilthead sea bream (Sparus aurata) (Teleostei) intestinal mucus: glycoprotein profile and bacterial adhesion. Parasitol Res 112: 567-576.
30. Torrecillas S, Makol A, Caballero MJ, Montero D, Ginés R, et al. (2011) Improved feed utilization, intestinal mucus production and immune parameters in sea bass (Dicentrarchus labrax) fed mannan oligosaccharides (MOS). Aquaculture Nutr 17: 223-233.
31. Micallef G, Bickerdike R, Reiff C, Fernandes J, Bowman A, et al. (2012) Exploring the transcriptome of Atlantic salmon (Salmo salar) skin, a major defense organ. Mar Biotechnol 14: 559-569.
32. Lang T, Alexandersson M, Hansson GC, Samuelsson T, (2004) Bioinformatic identification of polymerizing and transmembrane mucins in the puffer fish Fugu rubripes. Glycobiology 14: 521-527.
33. Sers C, Kirsch K, Rothbacher U, Riethmuller G, Johnson JP, (1993) Genomic organization of the melanoma-associated glycoprotein muc18- Implications for the evolution of the immunoglobulin domains. Proc Natl Acad Sci USA 90: 8514-8518.
34. Rothberg BEG, Bracken MB, Rimm DL, (2009) Tissue biomarkers for prognosis in cutaneous melanoma: A systematic review and meta-analysis. J Natl Cancer Inst 101: 452-474.
35. Williams SJ, Wreschner DH, Tran M, Eyre HJ, Sutherland GR, et al. (2001) MUC13, a novel human cell surface mucin expressed by epithelial and hemopoietic cells. J Biol Chem 276: 18327-18336.
36. Walsh MD, Young JP, Leggett BA, Williams SH, Jass JR, et al. (2007) The MUC13 cell surface mucin is highly expressed by human colorectal carcinomas. Hum Pathol 38: 883-892.
37. Chauhan SC, Vannatta K, Ebeling MC, Vinayek N, Watanabe A, et al. (2009) Expression and functions of transmembrane mucin MUC13 in ovarian cancer. Cancer Res 69: 765-774.
38. Shimamura T, Ito H, Shibahara J, Watanabe A, Hippo Y, et al. (2005) Overexpression of MUC13 is associated with intestinal-type gastric cancer. Cancer Sci 96: 265-273.
39. Maher DM, Gupta BK, Nagata S, Jaggi M, Chauhan SC, (2011) Mucin 13: Structure, function, and potential roles in cancer pathogenesis. Mol Cancer Res 9: 531-537.
40. Sheng YH, Lourie R, Linden SK, Jeffery PL, Roche D, et al. (2011) The MUC13 cell-surface mucin protects against intestinal inflammation by inhibiting epithelial cell apoptosis. Gut 60: 1661-1670.
41. Chen Y, Zhao YH, Kalaslavadi TB, Hamati E, Nehrke K, et al. (2004) Genome-wide search and identification of a novel gel-forming mucin MUC19/Muc19 in glandular tissues. Am J Respir Cell Mol Biol 30: 155-165.
42. Fänge T, Grove D (1979) Digestion. In: Hoar WS, Randall DJ, Brett JR, editors. Fish Physiology, Vol.8 Bioenergetics and growth. New York, USA: Academic Press Inc. 161-260.
43. Menzies M, Reverter A, Andronicos N, Hunt P, Windon R, et al. (2010) Nematode challenge induces differential expression of oxidant, antioxidant and mucous genes down the longitudinal axis of the sheep gut. Parasite Immunol 32: 36-46.
44. van der Marel M, Adamek M, González SF, Frost P, Rombout JHWM, et al. (2012) Molecular cloning and expression of two β-defensin and two mucin genes in common carp (Cyprinus carpio L.) and their up-regulation after β-glucan feeding. Fish Shellfish Immunol 32: 494-501.
45. Velcich A, Yang WC, Heyer J, Fragale A, Nicholas C, et al. (2002) Colorectal cancer in mice genetically deficient in the mucin Muc2. Science 295: 1726-1729.
46. McGuckin MA, Linden SK, Sutton P, Florin TH, (2011) Mucin dynamics and enteric pathogens. Nat Rev Micro 9: 265-278.
47. Artis D, Grencis RK, (2008) The intestinal epithelium: sensors to effectors in nematode infection. Mucosal Immunol 1: 252-264.
48. Rinaldi M, Dreesen L, Hoorens P, Li R, Claerebout E, et al. (2011) Infection with the gastrointestinal nematode Ostertagia ostertagi in cattle affects mucus biosynthesis in the abomasum. Vet Res 42: 61.
49. Soga K, Yamauchi J, Kawai Y, Yamada M, Uchikawa R, et al. (2008) Alteration of the expression profiles of acidic mucin, sialytransferase, and sulfotransferases in the intestinal epithelium of rats infected with the nematode Nippostrongylus brasiliensis. Parasitol Res 103: 1427-1434.
50. Fujino T, Fried B, (1993) Echinostoma caproni and Echinostoma trivolvis alter the binding of glycoconjugates in the intestinal-mucosa of c3h mice as determined by lectin histochemistry. J Helminthol 67: 179-188.
51. Steinberg SE, Banwell JG, Yardley JH, Keusch GT, Hendrix TR, (1975) Comparison of secretory and histological effects of Shigella and Cholera enterotoxins in rabbit jejunum. Gastroenterol 68: 309-317.
52. Sachdev HPS, Chadha V, Malhotra V, Verghese A, Puri RK, (1993) Rectal histopathology in endemic Shigella and Salmonella diarrhea. J Pediatr Gastroenterol Nutr 16: 33-38.
53. Lambert ME, Schofield PF, Ironside AG, Mandal BK, (1979) Campylobacter colitis. Br Med J 1: 857-859.
54. Bergstrom KSB, Guttman JA, Rumi M, Ma CX, Bouzari S, et al. (2008) Modulation of intestinal goblet cell function during infection by an attaching and effacing bacterial pathogen. Infect Immun 76: 796-811.
55. Fleurance R, Sauvegrain C, Marques A, Le Breton A, Guereaud C, et al. (2008) Histopathological changes caused by Enteromyxum leei infection in farmed sea bream Sparus aurata. Dis Aquat Org 79: 219-228.
56. Redondo MJ, Álvarez-Pellitero P, (2010) Carbohydrate patterns in the digestive tract of Sparus aurata L. and Psetta maxima (L.) (Teleostei) parasitized by Enteromyxum leei and E. scophthalmi (Myxozoa). Parasitol Int 59: 445-453.
57. Bosi G, Arrighi S, Di Giancamillo A, Domeneghini C, (2005) Histochemistry of glycoconjugates in mucous cells of Salmo trutta uninfected and naturally parasitized with intestinal helminths. Dis Aquat Org 64: 45-51.
58. Dezfuli BS, Pironi F, Campisi M, Shinn AP, Giari L, (2010) The response of intestinal mucous cells to the presence of enteric helminths: their distribution, histochemistry and fine structure. J Fish Dis 33: 481-488.
59. Bermúdez R, Faílde LD, Losada AP, Álvarez-Pellitero P, Quiroga MI (2009) Morphological and ultrastructural studies on enteromyxosis of turbot (Psetta maxima L.). Diseases of Fish and Shellfish, 14th European Association of Fish Pathologists International Conference. Prague, Czech Republic: HALAMA Publishing House, Czech Republic. 17 p.
60. Lien KA, Sauer WC, He JM, (2001) Dietary influences on the secretion into and degradation of mucin in the digestive tract of monogastric animals and humans. J Anim Feed Sci 10: 223-245.
61. Hino S, Takemura N, Sonoyama K, Morita A, Kawagishi H, et al. (2012) Small intestinal goblet cell proliferation induced by ingestion of soluble and insoluble dietary fiber is characterized by an increase in sialylated mucins in rats. J Nutr 142: 1429-1436.
62. Gaudier E, Jarry A, Blottiere HM, de Coppet P, Buisine MP, et al. (2004) Butyrate specifically modulates MUC gene expression in intestinal epithelial goblet cells deprived of glucose. Am J Physiol Gastrointest Liver Physiol 287: G1168-G1174.
63. Burger-van Paassen N, Vincent A, Puiman PJ, van der Sluis M, Bouma J, et al. (2009) The regulation of intestinal mucin MUC2 expression by short-chain fatty acids: implications for epithelial protection. Biochem J 420: 211-219.
64. Dykstra NS, Hyde L, Adawi D, Kulik D, Ahrne S, et al. (2011) Pulse probiotic administration induces repeated small intestinal Muc3 expression in rats. Pediatr Res 69: 206-211.
65. Smith AG, O'Doherty JV, Reilly P, Ryan MT, Bahar B, et al. (2011) The effects of laminarin derived from Laminaria digitata on measurements of gut health: selected bacterial populations, intestinal fermentation, mucin gene expression and cytokine gene expression in the pig. Br J Nutr 105: 669-677.
66. Martínez-Maqueda D, Miralles B, De Pascual-Teresa S, Reverón I, Muñoz R, et al. (2012) Food-derived peptides stimulate mucin secretion and gene expression in intestinal cells. J Agric Food Chem 60: 8600-8605.
67. Lee SY, Lee HJ, Sikder M, Shin HD, Kim JH, et al. (2012) Resveratrol inhibits mucin gene expression, production and secretion from airway epithelial cells. Phytother Res 26: 1082-1087.
68. Li N, Li Q, Zhou XD, Kolosov VP, Perelman JM, (2012) The effect of quercetin on human neutrophil elastase-induced mucin5AC expression in human airway epithelial cells. Int Immunopharmacol 14: 195-201.
69. Andrianifahanana M, Moniaux N, Batra SK, (2006) Regulation of mucin expression: Mechanistic aspects and implications for cancer and inflammatory diseases. Biochim Biophys Acta. Reviews on Cancer 1765: 189-222.
70. Moncada DM, Kammanadiminti SJ, Chadee K, (2003) Mucin and toll-like receptors in host defense against intestinal parasites. Trends Parasitol 19: 305-311.
71. Theodoropoulos G, Carraway KL, (2007) Molecular signaling in the regulation of mucins. J Cell Biochem 102: 1103-1116.
72. Lee KD, Guk SM, Chai JY, (2010) Toll-like receptor 2 and Muc2 expression on human intestinal epithelial cells by Gymnophalloides seoi adult antigen. J Parasitol 96: 58-66.
73. Skoog EC, Sjoling A, Navabi N, Holgersson J, Lundin SB, et al. (2012) Human gastric mucins differently regulate Helicobacter pylori proliferation, gene expression and interactions with host cells. PLoS ONE 7: e36378.
74. Linden SK, Florin THJ, McGuckin MA, (2008) Mucin dynamics in intestinal bacterial infection. PLoS ONE 3: e3952.
75. Sitjà-Bobadilla A, Calduch-Giner J, Saera-Vila A, Palenzuela O, Álvarez-Pellitero P, et al. (2008) Chronic exposure to the parasite Enteromyxum leei (Myxozoa: Myxosporea) modulates the immune response and the expression of growth, redox and immune relevant genes in gilthead sea bream, Sparus aurata L. Fish Shellfish Immunol. 24: 610-619.
76. Álvarez-Pellitero P (2011) Mucosal Intestinal Immunity and Response to Parasite Infections in Ectothermic Vertebrates. Immunology and Immune System Disorders, Nova Science Publishers, Inc. 108 p.
77. Harikrishnan R, Kim MC, Kim JS, Balasundaram C, Heo MS, (2011) Probiotics and herbal mixtures enhance the growth, blood constituents, and nonspecific immune response in Paralichthys olivaceus against Streptococcus parauberis Fish Shellfish Immunol. 31: 310-317.
78. Sitjà-Bobadilla A, Peña-Llopis S, Gómez-Requeni P, Medale F, Kaushik S, et al. (2005) Effect of fish meal replacement by plant protein sources on non-specific defence mechanisms and oxidative stress in gilthead sea bream (Sparus aurata). Aquaculture 249: 387-400.
79. Montero D, Mathlouthi F, Tort L, Afonso JM, Torrecillas S, et al. (2010) Replacement of dietary fish oil by vegetable oils affects humoral immunity and expression of pro-inflammatory cytokines genes in gilthead sea bream Sparus aurata Fish Shellfish Immunol. 29: 1073-1081.