Expressed IgH μ and τ transcripts share diversity segment in ranched Thunnus orientalis

Developmental and Comparative Immunology

Volumn 43, Issue 1, 2014, Pages 76-86

  Mashoof, Sara ^a   Pohlenz, Camilo ^b   Chen, Patricia L ^a   Deiss, Thaddeus C ^a   Gatlin, Delbert ^b   Buentello, Alejandro ^c   Criscitiello, Michael F ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

^c Schillinger Genetics   (United States)

Author keywords

Evolution; IgZ T; Immunoglobulin; Isotype exclusion; Tuna

Indexed keywords

COMPLEMENTARY DNA; IMMUNOGLOBULIN; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN M; IMMUNOGLOBULIN T; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; AQUACULTURE; ARTICLE; CELL LINEAGE; COMPLEMENTARITY DETERMINING REGION; CONTROLLED STUDY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE SEQUENCE; GENETIC RECOMBINATION; GENETIC VARIABILITY; HUMORAL IMMUNITY; IMMUNOGLOBULIN GENE; MOLECULAR CLONING; NEIGHBOR JOINING METHOD; NONHUMAN; NUCLEOTIDE SEQUENCE; PERCIFORMES; PHYLOGENY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; THUNNUS ORIENTALIS; CLONE; GENE REARRANGEMENT; GENE STRUCTURE; GENETIC TRANSCRIPTION; IMMUNOGLOBULIN VARIABLE REGION; MULTIGENE FAMILY; TUNA;

PERCIFORMES; SCOMBRIDAE; THUNNUS ORIENTALIS;

EVOLUTION; IGZ/T; IMMUNOGLOBULIN; ISOTYPE EXCLUSION; TUNA;

AMINO ACID SEQUENCE; ANIMALS; CELLS, CULTURED; GENE REARRANGEMENT, B-LYMPHOCYTE, HEAVY CHAIN; IMMUNITY, HUMORAL; IMMUNOGLOBULIN HEAVY CHAINS; IMMUNOGLOBULIN M; IMMUNOGLOBULIN VARIABLE REGION; IMMUNOGLOBULINS; MOLECULAR SEQUENCE DATA; PHYLOGENY; SEQUENCE HOMOLOGY, NUCLEIC ACID; TRANSCRIPTOME; TUNA; VACCINES;

EID: 84888091751     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2013.10.015     Document Type: Article

References (72)

1. Amemiya C.T., Alfoldi J., Lee A.P., Fan S., Philippe H., Maccallum I., Braasch I., Manousaki T., Schneider I., Rohner N., Organ C., Chalopin D., Smith J.J., Robinson M., Dorrington R.A., Gerdol M., Aken B., Biscotti M.A., Barucca M., Baurain D., Berlin A.M., Blatch G.L., Buonocore F., Burmester T., Campbell M.S., Canapa A., Cannon J.P., Christoffels A., De Moro G., Edkins A.L., Fan L., Fausto A.M., Feiner N., Forconi M., Gamieldien J., Gnerre S., Gnirke A., Goldstone J.V., Haerty W., Hahn M.E., Hesse U., Hoffmann S., Johnson J., Karchner S.I., Kuraku S., Lara M., Levin J.Z., Litman G.W., Mauceli E., Miyake T., Mueller M.G., Nelson D.R., Nitsche A., Olmo E., Ota T., Pallavicini A., Panji S., Picone B., Ponting C.P., Prohaska S.J., Przybylski D., Saha N.R., Ravi V., Ribeiro F.J., Sauka-Spengler T., Scapigliati G., Searle S.M., Sharpe T., Simakov O., Stadler P.F., Stegeman J.J., Sumiyama K., Tabbaa D., Tafer H., Turner-Maier J., van Heusden P., White S., Williams L., Yandell M., Brinkmann H., Volff J.N., Tabin C.J., Shubin N., Schartl M., Jaffe D.B., Postlethwait J.H., Venkatesh B., Di Palma F., Lander E.S., Meyer A., Lindblad-Toh K. The African coelacanth genome provides insights into tetrapod evolution. Nature 2013, 496:311-316.
2. Barr M., Mott K., Zwollo P. Defining terminally differentiating B cell populations in rainbow trout immune tissues using the transcription factor XbpI. Fish Shellfish Immunol. 2011, 31:727-735.
3. Barreto Vasco M., Qiang Pan-Hammarstrom Y.Z., Hammarstrom Lennart, Misulovin Ziva, Nussenzweig M.C. AID from bony fish catalyzes class switch recombination. JEM 2005, 202:733-738.
4. Bengten E., Quiniou S.M., Stuge T.B., Katagiri T., Miller N.W., Clem L.W., Warr G.W., Wilson M. The IgH locus of the channel catfish, Ictalurus punctatus, contains multiple constant region gene sequences: different genes encode heavy chains of membrane and secreted IgD. J. Immunol. 2002, 169:2488-2497.
5. Bengten E., Clem L.W., Miller N.W., Warr G.W., Wilson M. Channel catfish immunoglobulins: repertoire and expression. Dev. Comp. Immunol. 2006, 30:77-92.
6. Block B.A., Dewar H., Blackwell S.B., Williams T.D., Prince E.D., Farwell C.J., Boustany A., Teo S.L.H., Seitz A., Walli A., Fudge D. Migratory movements, depth preferences, and thermal biology of Atlantic bluefin tuna. Science 2001, 293:1310-1314.
7. Brodeur P.H., Riblet R. The immunoglobulin heavy chain variable region (Igh-V) locus in the mouse. I. One hundred Igh-V genes comprise seven families of homologous genes. Eur. J. Immunol. 1984, 14:922-930.
8. Castro R., Jouneau L., Pham H.P., Bouchez O., Giudicelli V., Lefranc M.P., Quillet E., Benmansour A., Cazals F., Six A., Fillatreau S., Sunyer O., Boudinot P. Teleost fish mount complex clonal IgM and IgT responses in spleen upon systemic viral infection. PLoS Pathog. 2013, 9:e1003098.
9. Colquitt S.E., Munday B.L., Daintith W. Pathological findings in southern bluefin tuna, Thunnus maccoyii (Castelnau), infected with Cardicola forsteri (Cribb, Daintith & Munday, 2000) (Digenea: Sanguinicolidae), a blood fluke. J. Fish Dis. 2001, 24:225-229.
10. Criscitiello M.F., Flajnik M.F. Four primordial immunoglobulin light chain isotypes, including lambda and kappa, identified in the most primitive living jawed vertebrates. Eur. J. Immunol. 2007, 37:2683-2694.
11. Danilova N., Amemiya C.T. Going adaptive: the saga of antibodies. Ann. N.Y. Acad. Sci. 2009, 1168:130-155.
12. Danilova N.B.J., Jekosch K., Steiner L.A. The immunoglobulin heavy-chain locus in zebrafish: identification and expression of a previously unknown isotype, immunoglobulin Z. Nat. Immunol. 2005, 6:295-302.
13. Danilova N., Bussmann J., Jekosch K., Steiner L.A. The immunoglobulin heavy-chain locus in zebrafish: identification and expression of a previously unknown isotype, immunoglobulin Z. Nat. Immunol. 2005, 6:295-302.
14. Danilova N., Saunders H.L., Ellestad K.K., Magor B.G. The zebrafish IgH locus contains multiple transcriptional regulatory regions. Dev. Comp. Immunol. 2011, 35:352-359.
15. Davis M.M. The evolutionary and structural 'logic' of antigen receptor diversity. Semin. Immunol. 2004, 16:239-243.
16. Edholm E.S., Bengten E., Stafford J.L., Sahoo M., Taylor E.B., Miller N.W., Wilson M. Identification of two IgD+ B cell populations in channel catfish, Ictalurus punctatus. J. Immunol. 2010, 185:4082-4094.
17. Emanuelsson O., Brunak S., Von Heijne G., Nielsen H. Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2007, 2:953-971.
18. Fillatreau S., Six A., Magadan S., Castro R., Sunyer J.O., Boudinot P. The astonishing diversity of Ig classes and B cell repertoires in teleost fish. Front. Immunol. 2013, 4:28.
19. Flajnik M.F., Rumfelt L.L. Early and natural antibodies in non-mammalian vertebrates. Curr. Top. Microbiol. Immunol. 2000, 252:233-240.
20. Fromentin J.M., Powers J.E. Atlantic bluefin tuna: population dynamics, ecology, fisheries and management. Fish Fish. 2005, 6:281-306.
21. Gambon-Deza F., Sanchez-Espinel C., Magadan-Mompo S. Presence of an unique IgT on the IGH locus in three-spined stickleback fish (Gasterosteus aculeatus) and the very recent generation of a repertoire of VH genes. Dev. Comp. Immunol. 2010, 34:114-122.
22. Gomez D.K., Mori K., Okinaka Y., Nakai T., Park S.C. Trash fish can be a source of betanodaviruses for cultured marine fish. Aquaculture 2010, 302:158-163.
23. Hansen J.D., Landis E.D., Phillips R.B. Discovery of a unique Ig heavy-chain isotype (IgT) in rainbow trout: implications for a distinctive B cell developmental pathway in teleost fish. Proc. Natl. Acad. Sci. USA 2005, 102:6919-6924.
24. Hansen John D., L E.D., Phillips Ruth B. Discovery of a unique Ig heavy-chain isotype (IgT) in rainbow trout: implications for a distinctive B cell developmental pathway in teleost fish. PNAS 2005, 102:6919-6924.
25. Hayward C.J., Bott N.J., Nowak B.F. Seasonal epizootics of sea lice, Caligus spp., on southern bluefin tuna, Thunnus maccoyii (Castelnau), in a long-term farming trial. J. Fish Dis. 2009, 32:101-106.
26. Hikima J., Jung T.S., Aoki T. Immunoglobulin genes and their transcriptional control in teleosts. Dev. Comp. Immunol. 2011, 35:924-936.
27. Hohman V.S., Stewart S.E., Rumfelt L.L., Greenberg A.S., Avila D.W., Flajnik M.F., Steiner L.A. J chain in the nurse shark: implications for function in a lower vertebrate. J. Immunol. 2003, 170:6016-6023.
28. Hu Y.L., Xiang L.X., Shao J.Z. Identification and characterization of a novel immunoglobulin Z isotype in zebrafish: implications for a distinct B cell receptor in lower vertebrates. Mol. Immunol. 2010, 47:738-746.
29. Jones D.T., Taylor W.R., Thornton J.M. The rapid generation of mutation data matrices from protein sequences. CABIOS 1992, 8:275-282.
30. Jørgensen T.Ø., S J. Immunoglobulin D (IgD) of Atlantic cod has a unique structure. Immunogenetics 2000, 51:452-461.
31. Jusup M., Klanjscek T., Matsuda H., Kooijman S.A. A full lifecycle bioenergetic model for bluefin tuna. PLoS One 2011, 6:e21903.
32. Kaattari S., Evans D., Klemer J. Varied redox forms of teleost IgM: an alternative to isotypic diversity?. Immunol. Rev. 1998, 166:133-142.
33. Koichiro Tamura, D.P., Peterson, N., Stecher, G., Nei, M., Kumar, S. 2011. Molecular evolutionary genetics analysis, Authors:.
34. Kwong P.D., Wilson I.A. HIV-1 and influenza antibodies: seeing antigens in new ways. Nat. Immunol. 2009, 10:573-578.
35. Lam S.H., Chua H.L., Gong Z., Lam T.J., Sin Y.M. Development and maturation of the immune system in zebrafish, Danio rerio: a gene expression profiling, in situ hybridization and immunological study. Dev. Comp. Immunol. 2004, 28:9-28.
36. Lefranc M.P., Pommie C., Ruiz M., Giudicelli V., Foulquier E., Truong L., Thouvenin-Contet V., Lefranc G. IMGT unique numbering for immunoglobulin and T cell receptor variable domains and Ig superfamily V-like domains. Dev. Comp. Immunol. 2003, 27:55-77.
37. Lesk A.M., Chothia C. Evolution of proteins formed by beta-sheets. II. The core of the immunoglobulin domains. J. Mol. Biol. 1982, 160:325-342.
38. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
39. Macmurray E., Barr M., Bruce A., Epp L., Zwollo P. Alternative splicing of the trout Pax5 gene and identification of novel B cell populations using Pax5 signatures. Dev. Comp. Immunol. 2013, 41:270-281.
40. Magadan-Mompo S., Sanchez-Espinel C., Gambon-Deza F. Immunoglobulin heavy chains in medaka (Oryzias latipes). BMC Evol. Biol. 2011, 11:165.
41. Mashoof S., Goodroe A., Du C.C., Eubanks J.O., Jacobs N., Steiner J.M., Tizard I., Suchodolski J.S., Criscitiello M.F. Ancient T-independence of mucosal IgX/A: gut microbiota unaffected by larval thymectomy in Xenopus laevis. Mucosal Immunol. 2013, 6:358-368.
42. McLellan J.S., Pancera M., Carrico C., Gorman J., Julien J.P., Khayat R., Louder R., Pejchal R., Sastry M., Dai K., O'Dell S., Patel N., Shahzad-ul-Hussan S., Yang Y., Zhang B., Zhou T., Zhu J., Boyington J.C., Chuang G.Y., Diwanji D., Georgiev I., Kwon Y.D., Lee D., Louder M.K., Moquin S., Schmidt S.D., Yang Z.Y., Bonsignori M., Crump J.A., Kapiga S.H., Sam N.E., Haynes B.F., Burton D.R., Koff W.C., Walker L.M., Phogat S., Wyatt R., Orwenyo J., Wang L.X., Arthos J., Bewley C.A., Mascola J.R., Nabel G.J., Schief W.R., Ward A.B., Wilson I.A., Kwong P.D. Structure of HIV-1 gp120 V1/V2 domain with broadly neutralizing antibody PG9. Nature 2011, 480:336-343.
43. Mladineo I., Block B.A. Expression of Hsp70, Na+/K+ ATP-ase, HIF-1 alpha, IL-1 beta and TNF-alpha in captive Pacific bluefin tuna (Thunnus orientalis) after chronic warm and cold exposure. J. Exp. Mar. Biol. Ecol. 2009, 374:51-57.
44. Olivieri D., Faro J., von Haeften B., Sanchez-Espinel C., Gambon-Deza F. An automated algorithm for extracting functional immunologic V-genes from genomes in jawed vertebrates. Immunogenetics 2013, 65:691-702.
45. Olsen M.M., Kania P.W., Heinecke R.D., Skjoedt K., Rasmussen K.J., Buchmann K. Cellular and humoral factors involved in the response of rainbow trout gills to Ichthyophthirius multifiliis infections: molecular and immunohistochemical studies. Fish Shellfish Immunol. 2011, 30:859-869.
46. Ottolenghi F. Capture-based aquaculture of blue-fin tuna. Capture-Based Aquaculture 2008, 169-182. Food and Agriculture Organization of the United Nations, Rome. A. Lovatelli, P. Holthus (Eds.).
47. Page, R.D., 2002. Visualizing phylogenetic trees using TreeView. In: Baxevanis, A.D., et al. (Eds.), Current Protocols in Bioinformatics, Unit 6 2. Chapter 6.
48. Pascual V., Capra J.D. Human immunoglobulin heavy-chain variable region genes: organization, polymorphism, and expression. Adv. Immunol. 1991, 49:1-74.
49. Ramirez-Gomez F., Greene W., Rego K., Hansen J.D., Costa G., Kataria P., Bromage E.S. Discovery and characterization of secretory IgD in rainbow trout: secretory IgD is produced through a novel splicing mechanism. J. Immunol. 2012, 188:1341-1349.
50. Ryo S., Wijdeven R.H.M., Tyagi A., Hermsen T., Kono T., Karunasagar I., Rombout J.H.W.M., Sakai M., Verburg-van Kemenade B.M.L., Savan R. Common carp have two subclasses of bonyfish specific antibody IgZ showing differential expression in response to infection. Dev. Comp. Immunol. 2010, 34:1183-1190.
51. Salinas I., Zhang Y.A., Sunyer J.O. Mucosal immunoglobulins and B cells of teleost fish. Dev. Comp. Immunol. 2011, 35:1346-1365.
52. Aparicio Samuel, C J., Stupka Elia, Putnam Nik, C J.-M., Dehal Paramvir, Christoffels Alan, R S., Hoon Shawn, Smit Arian, Sollewijn Gelpke Maarten D., Roach Jared, O T., Ho Isaac Y., W M., Detter Chris, Verhoef Frans, Predki Paul, T A., Lucas Susan, Richardson Paul, Smith Sarah F., C M.S., Edwards Yvonne J.K., Doggett Norman, Z A., Tavtigian Sean V., Pruss Dmitry, B M., Evans Cheryl, Baden Holly, Powell Justin, G G., Rowen Lee, Hood Leroy, Tan Y.H., E G., Hawkins Trevor, Venkatesh Byrappa, R D., Brenner Sydney Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science 2002, 297:1301.
53. Savan R., Aman A., Nakao M., Watanuki H., Sakai M. Discovery of a novel immunoglobulin heavy chain gene chimera from common carp (Cyprinus carpio L.). Immunogenetics 2005, 57:458-463.
54. Savan R., Aman A., Sato K., Yamaguchi R., Sakai M. Discovery of a new class of immunoglobulin heavy chain from fugu. Eur. J. Immunol. 2005, 35:3320-3331.
55. Schorpp M., Bialecki M., Diekhoff D., Walderich B., Odenthal J., Maischein H.M., Zapata A.G., Boehm T. Conserved functions of Ikaros in vertebrate lymphocyte development: genetic evidence for distinct larval and adult phases of T cell development and two lineages of B cells in zebrafish. J. Immunol. 2006, 177:2463-2476.
56. Schwarz R., Dayhoff M. Matrices for detecting distant relationships. Atlas of Protein Sequences 1979, 353-358. National Biomedical Research Foundation. D. M (Ed.).
57. Tacchi L., Larragoite E., Salinas I. Discovery of J Chain in African lungfish (Protopterus dolloi, Sarcopterygii) using high throughput transcriptome sequencing: implications in mucosal immunity. PLoS One 2013, 8:e70650.
58. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28:2731-2739.
59. Tian J.Y., Sun B.J., Luo Y.P., Zhang Y.A., Nie P. Distribution of IgM, IgD and IgZ in mandarin fish, Siniperca chuatsi lymphoid tissues and their transcriptional changes after Flavobacterium columnare stimulation. Aquaculture 2009, 288:14-21.
60. Trede N.S., Langenau D.M., Traver D., Look A.T., Zon L.I. The use of zebrafish to understand immunity. Immunity 2004, 20:367-379.
61. Wakae K., Magor B.G., Saunders H., Nagaoka H., Kawamura A., Kinoshita K., Honjo T., Muramatsu M. Evolution of class switch recombination function in fish activation-induced cytidine deaminase, AID. Int. Immunol. 2006, 18:41-47.
62. Wang F., Ekiert D.C., Ahmad I., Yu W., Zhang Y., Bazirgan O., Torkamani A., Raudsepp T., Mwangi W., Criscitiello M.F., Wilson I.A., Schultz P.G., Smider V.V. Reshaping antibody diversity. Cell 2013, 153:1379-1393.
63. Watts M., Munday B.L., Burke C.M. Isolation and partial characterisation of immunoglobulin from southern bluefin tuna Thunnus maccoyii Castelnau. Fish Shellfish Immunol. 2001, 11:491-503.
64. Wiersma E.J., Chen F., Bazin R., Collins C., Painter R.H., Lemieux R., Shulman M.J. Analysis of IgM structures involved in J chain incorporation. J. Immunol. 1997, 158:1719-1726.
65. Wilson M., Bengten E., Miller N.W., Clem L.W., Du P.L., Warr G.W. A novel chimeric Ig heavy chain from a teleost fish shares similarities to IgD. Proc. Natl. Acad. Sci. USA 1997, 94:4593-4597.
66. Xiao F.S., Wang Y.P., Yan W., Chang M.X., Yao W.J., Xu Q.Q., Wang X.X., Gao Q., Nie P. Ig heavy chain genes and their locus in grass carp Ctenopharyngodon idella. Fish Shellfish Immunol. 2010, 29:594-599.
67. Xu J.L., Davis M.M. Diversity in the CDR3 region of V(H) is sufficient for most antibody specificities. Immunity 2000, 13:37-45.
68. Xu Z., Parra D., Gomez D., Salinas I., Zhang Y.A., von Gersdorff Jorgensen L., Heinecke R.D., Buchmann K., Lapatra S., Sunyer J.O. Teleost skin, an ancient mucosal surface that elicits gut-like immune responses. Proc. Natl. Acad. Sci. USA 2013, 110:13097-13102.
69. Zhang Y.A., Salinas I., Li J., Parra D., Bjork S., Xu Z., LaPatra S.E., Bartholomew J., Sunyer J.O. IgT, a primitive immunoglobulin class specialized in mucosal immunity. Nat. Immunol. 2010, 11:827-835.
70. Zhang Y.A., Salinas I., Oriol Sunyer J. Recent findings on the structure and function of teleost IgT. Fish Shellfish Immunol. 2011, 31:627-634.
71. Zhu C., Lee V., Finn A., Senger K., Zarrin A.A., Du Pasquier L., Hsu E. Origin of Immunoglobulin Isotype Switching. Curr. Biol. 2012, 22:872-880.
72. Zimmerman A.M., Moustafa F.M., Romanowski K.E., Steiner L.A. Zebrafish immunoglobulin IgD: unusual exon usage and quantitative expression profiles with IgM and IgZ/T heavy chain isotypes. Mol. Immunol. 2011, 48:2220-2223.