Trans-species polymorphism at antimicrobial innate immunity cathelicidin genes of Atlantic cod and related species

PeerJ

Volumn 2015, Issue 5, 2015, Pages

  Halldórsdóttir, Katrín ^a   Árnason, Einar ^a  

^a UNIVERSITY OF ICELAND   (Iceland)

Author keywords

Atlantic cod; Balancing selection; Cathelicidin; Gadids; Innate immunity; Trans species polymorphism

Indexed keywords

CATHELICIDIN; COMPLEMENTARY DNA; GENOMIC DNA; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

AMINO ACID SEQUENCE; ARTICLE; ATLANTIC COD; BAYES THEOREM; BOREOGADUS SAIDA; CLONE; CODON; CONSENSUS SEQUENCE; DISCRIMINANT ANALYSIS; EXON; FISH; GADUS CHALCOGRAMMUS; GADUS MACROCEPHALUS; GADUS OGAC; GENE; GENE CLUSTER; GENE CONVERSION; GENE FREQUENCY; GENETIC POLYMORPHISM; GENETIC SELECTION; GENETIC VARIABILITY; INNATE IMMUNITY CATHELICIDIN GENE; MAXIMUM LIKELIHOOD METHOD; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; PARALOGY; POLYMERASE CHAIN REACTION; POPULATION DIFFERENTIATION; PROTEIN SECONDARY STRUCTURE; SEQUENCE ALIGNMENT; TRANS SPECIES POLYMORPHISM;

GADIDAE; GADUS MORHUA; VERTEBRATA;

EID: 84930658070     PISSN: None     EISSN: 21678359     Source Type: Journal    
DOI: 10.7717/peerj.976     Document Type: Article

References (90)

1. Árnason E. 2004. Mitochondrial cytochrome b DNA variation in the high fecundity Atlantic cod: Trans-Atlantic clines and shallow gene-genealogy. Genetics 166:1871-1885 DOI 10.1534/genetics.166.4.1871.
2. Árnason E, Halldórsdóttir K. 2015. Nucleotide variation and balancing selection at the Ckma gene in Atlantic cod: analysis with multiple merger coalescent models. PeerJ 3:e786 DOI 10.7717/peerj.786.
3. Árnason E, Paĺsson S. 1996. Mitochondrial cytochrome b DNA sequence variation of Atlantic cod, Gadus morhua, from Norway. Molecular Ecology 5:715-724 DOI 10.1111/j.1365-294X.1996.tb00368.x.
4. Bakker EG, Toomajian C, Kreitman M, Bergelson J. 2006. A genome-wide survey of R gene polymorphisms in Arabidopsis. The Plant Cell Online 18(8):1803-1818 DOI 10.1105/tpc.106.042614.
5. Bals R, Wilson JM. 2003. Cathelicidins-a family of multifunctional antimicrobial peptides. Cellular and Molecular Life Sciences 60(4):711-720 DOI 10.1007/s00018-003-2186-9.
6. Barreiro LB, Quintana-Murci L. 2010. From evolutionary genetics to human immunology: how selection shapes host defence genes. Nature Review Genetics 11(01):17-30 DOI 10.1038/nrg2698.
7. Beitz E. 2000. TEX shade: shading and labeling multiple sequence alignments using LATEX2ε. Bioinformatics 16:135-139 DOI 10.1093/bioinformatics/16.2.135.
8. Birkner M, Blath J, Eldon B. 2013. Statistical properties of the site-frequency spectrum associated with Λ-coalescents. Genetics 195:1037-1053 DOI 10.1534/genetics.113.156612.
9. Bowman S, Hubert S, Higgins B, Stone C, Kimball J, Borza T, Bussey JT, Simpson G, Kozera C, Curtis BA, Hall JR, Hori TS, Feng CY, Rise M, Booman M, Gamperl AK, Trippel E, Symonds J, Johnson SC, Rise ML. 2011. An integrated approach to gene discovery and marker development in Atlantic cod (Gadus morhua). Marine Biotechnology 13(2):242-255 DOI 10.1007/s10126-010-9285-z.
10. Broekman DC, Frei DM, Gylfason GA, Steinarsson A, Jörnvall H, Agerberth B, Gudmundsson GH, Maier VH. 2011a. Cod cathelicidin: isolation of the mature peptide, cleavage site characterisation and developmental expression. Developmental & Comparative Immunology 35(3):296-303 DOI 10.1016/j.dci.2010.10.002.
11. Broekman DC, Zenz A, Gudmundsdottir BK, Lohner K, Maier VH, Gudmundsson GH. 2011b. Functional characterization of codCath, the mature cathelicidin antimicrobial peptide from Atlantic cod (Gadus morhua). Peptides 32(10):2044-2051 DOI 10.1016/j.peptides.2011.09.012.
12. Carr SM, Kivlichan DS, Pepin P, Crutcher DC. 1999. Molecular systematics of Gadid fishes: implications for the biogeographic origins of Pacific species. Canadian Journal of Zoology 77(1):19-26 DOI 10.1139/z98-194.
13. Charif D, Lobry J. 2007. SeqinR 1.0-2: a contributed package to the R project for statistical computing devoted to biological sequences retrieval and analysis. In: Bastolla U, Porto M, Roman H, Vendruscolo M, eds. Structural approaches to sequence evolution: molecules, networks, populations, Biological and medical physics, biomedical engineering. New York: Springer Verlag, 207-232.
14. Charlesworth D. 2006. Balancing selection and its effects on sequences in nearby genome regions. PLoS Genetics 2(4):e64 DOI 10.1371/journal.pgen.0020064.
15. Chen J-M, Cooper DN, Chuzhanova N, Férec C, Patrinos GP. 2007. Gene conversion: mechanisms, evolution and human disease. Nature Review Genetics 8:762-775 DOI 10.1038/nrg2193.
16. Clark AG. 1997. Neutral behavior of shared polymorphism. Proceedings of the National Academy of Sciences of the United States of America 94(15):7730-7734 DOI 10.1073/pnas.94.15.7730.
17. Clarke B. 1962. Balanced polymorphism and the diversity of sympatric species. In: Nichols D, ed. Taxonomy and geography. Oxford: Systematics Association, 47-70.
18. Coulson MW, Marshall HD, Pepin P, Carr SM. 2006. Mitochondrial genomics of gadine fishes: implications for taxonomy and biogeographic origins from whole-genome data sets. Genome 49:1115-1130 DOI 10.1139/g06-083.
19. Cunningham KM, Canino MF, Spies IB, Hauser L. 2009. Genetic isolation by distance and localized fjord population structure in Pacific cod (Gadus macrocephalus): limited effective dispersal in the northeastern Pacific Ocean. Canadian Journal of Fisheries and Aquatic Science 66:153-166 DOI 10.1139/F08-199.
20. Dawson H, Loveland J, Pascal G, Gilbert J, Uenishi H, Mann K, Sang Y, Zhang J, Carvalho-Silva D, Hunt T, Hardy M, Hu Z, Zhao S-H, Anselmo A, Shinkai H, Chen C, Badaoui B, Berman D, Amid C, Kay M, Lloyd D, Snow C, Morozumi T, Cheng RP-Y, Bystrom M, Kapetanovic R, Schwartz J, Kataria R, Astley M, Fritz E, Steward C, Thomas M, Wilming L, Toki D, Archibald A, Bed'Hom B, Beraldi D, Huang T-H, Ait-Ali T, Blecha F, Botti S, Freeman T, Giuffra E, Hume D, Lunney J, Murtaugh M, Reecy J, Harrow J, Rogel-Gaillard C, Tuggle C. 2013. Structural and functional annotation of the porcine immunome. BMC Genomics 14(1):332 DOI 10.1186/1471-2164-14-332.
21. Delport W, Poon AFY, Frost SDW, Kosakovsky Pond SL. 2010. Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 26(19):2455-2457 DOI 10.1093/bioinformatics/btq429.
22. Dray S, Dufour A. 2007. The ade4 package: implementing the duality diagram for ecologists. Journal of Statistical Software 22:1-20.
23. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32(5):1792-1797 DOI 10.1093/nar/gkh340.
24. Eimes J, Townsend A, Sepil I, Nishiumi I, Satta Y. 2015. Patterns of evolution of MHC class II genes of crows (Corvus) suggest trans-species polymorphism. PeerJ 3:e853 DOI 10.7717/peerj.853.
25. Eirí{dotless}ksson GM, Árnason E. 2013. Spatial and temporal microsatellite variation in spawning Atlantic cod, Gadus morhua, around Iceland. Canadian Journal of Fisheries and Aquattic Sciences 70(8):1151-1158 DOI 10.1139/cjfas-2012-0494.
26. Ewing B, Green P. 1998. Basecalling of automated sequencer traces using phred. II. Error probabilities. Genome Research 8:186-194 DOI 10.1101/gr.8.3.175.
27. Ewing B, Hillier L, Wendl M, Green P. 1998. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Research 8:175-185 DOI 10.1101/gr.8.3.175.
28. Fan W, Kasahara M, Gutknecht J, Klein D, Mayer WE, Jonker M, Klein J. 1989. Shared class II MHC polymorphisms between humans and chimpanzees. Human Immunology 26(2):107-121 DOI 10.1016/0198-8859(89)90096-7.
29. Fernandes JMO, Ruangsri J, Kiron V. 2010. Atlantic cod piscidin and its diversification through positive selection. PLoS ONE 5(3):e9501 DOI 10.1371/journal.pone.0009501.
30. Flicek P, Amode MR, Barrell D, Beal K, Billis K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fitzgerald S, Gil L, Girón CG, Gordon L, Hourlier T, Hunt S, Johnson N, Juettemann T, Kähäri AK, Keenan S, Kulesha E, Martin FJ, Maurel T, McLaren WM, Murphy DN, Nag R, Overduin B, Pignatelli M, Pritchard B, Pritchard E, Riat HS, Ruffier M, Sheppard D, Taylor K, Thormann A, Trevanion SJ, Vullo A, Wilder SP, Wilson M, Zadissa A, Aken BL, Birney E, Cunningham F, Harrow J, Herrero J, Hubbard TJ, Kinsella R, Muffato M, Parker A, Spudich G, Yates A, Zerbino DR, Searle SM. 2014. Ensembl 2014. Nucleic Acids Research 42(D1):D749-D755 DOI 10.1093/nar/gkt1196.
31. Gao Z, Przeworski M, Sella G. 2015. Footprints of ancient-balanced polymorphisms in genetic variation data from closely related species. Evolution 69(2):431-446 DOI 10.1111/evo.12567.
32. Gordon D, Abajian C, Green P. 1998. Consed: a graphical tool for sequence finishing. Genome Research 8:195-202 DOI 10.1101/gr.8.3.195.
33. Gouy M, Guindon S, Gascuel O. 2010. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution 27(2):221-224 DOI 10.1093/molbev/msp259.
34. Gudmundsson GA, Agerberth B, Odeberg J, Bergman T, Olsson B, Salcedo R. 1996. The human gene FALL39 and processing of the cathelin precursor to the antibacterial peptide LL-37 in granulocytes. European Journal of Biochemistry 238:325-332 DOI 10.1111/j.1432-1033.1996.0325z.x.
35. Guindon S, Gascuel O. 2003. A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52:696-704 DOI 10.1080/10635150390235520.
36. Halldórsdóttir K, Árnason E. 2009. Multiple linked β and α globin genes in Atlantic cod: a PCR based strategy of genomic exploration. Marine Genomics 2:169-181 DOI 10.1016/j.margen.2009.10.001.
37. Hughes AL. 2002. Natural selection and the diversification of vertebrate immune effectors. Immunological Reviews 190(1):161-168 DOI 10.1034/j.1600-065X.2002.19012.x.
38. Jombart T, Ahmed I. 2011. Adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27:3070-3071 DOI 10.1093/bioinformatics/btr521.
39. Jońsdóttir Ó, Imsland A, Daní{dotless}elsdóttir A, Thorsteinsson V, Navdal G. 1999. Genetic differentiation among Atlantic cod in south and south-east Icelandic waters: synaptophysin (SypI) and haemoglobin (HbI) variation. Journal of Fish Biology 54:1259-1274 DOI 10.1111/j.1095-8649.1999.tb02053.x.
40. Källberg M, Wang H, Wang S, Peng J, Wang Z, Lu H, Xu J. 2012. Template-based protein structure modeling using the raptorx web server. Nature Protocols 7:1511-1522 DOI 10.1038/nprot.2012.085.
41. Kapralova KH, Gudbrandsson J, Reynisdottir S, Santos CB, Baltanás VC, Maier VH, Snorrason SS, Palsson A. 2013. Differentiation at the MHCIIα and Cath2 loci in sympatric Salvelinus alpinus resource morphs in lake Thingvallavatn. PLoS ONE 8(7):e69402 DOI 10.1371/journal.pone.0069402.
42. Kingman JFC. 1982. The coalescent. Stochastic Processes and their Applications 13:235-248 DOI 10.1016/0304-4149(82)90011-4.
43. Kosakovsky Pond SL, Frost SDW. 2005. Not so different after all: a comparison of methods for detecting amino acid sites under selection. Molecular Biology and Evolution 22(5):1208-1222 DOI 10.1093/molbev/msi105.
44. Kosakovsky Pond SL, Posada D, Gravenor MB, Woelk CH, Frost SDW. 2006. Automated phylogenetic detection of recombination using a genetic algorithm. Molecular Biology and Evolution 23(10):1891-1901 DOI 10.1093/molbev/msl051.
45. Lamb BC. 1984. The properties of meiotic gene conversion important in its effects on evolution. Heredity 53:113-138 DOI 10.1038/hdy.1984.68.
46. Leffler EM, Bullaughey K, Matute DR, Meyer WK, Ségurel L, Venkat A, Andolfatto P, Przeworski M. 2012. Revisiting an old riddle: What determines genetic diversity levels within species? PLoS Biology 10(9):e1001388 DOI 10.1371/journal.pbio.1001388.
47. Leffler EM, Gao Z, Pfeifer S, Ségurel L, Auton A, Venn O, Bowden R, Bontrop R, Wall JD, Sella G, Donnelly P, McVean G, Przeworski M. 2013. Multiple instances of ancient balancing selection shared between humans and chimpanzees. Science 339(6127):1578-1582 DOI 10.1126/science.1234070.
48. Lenz TL, Becker S. 2008. Simple approach to reduce (PCR) artefact formation leads to reliable genotyping of (MHC) and other highly polymorphic loci-implications for evolutionary analysis. Gene 427(1-2):117-123 DOI 10.1016/j.gene.2008.09.013.
49. Liao D. 1999. Concerted evolution: molecular mechanism and biological implications. American Journal of Human Genetics 64(1):24-30 DOI 10.1086/302221.
50. Librado P, Rozas J. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25(11):1451-1452 DOI 10.1093/bioinformatics/btp187.
51. Magnadottir B. 2010. Immunological control of fish diseases. Marine Biotechnology 12(4):361-379 DOI 10.1007/s10126-010-9279-x.
52. Maier VH, Dorn KV, Gudmundsdottir BK, Gudmundsson GH. 2008. Characterisation of cathelicidin gene family members in divergent fish species. Molecular Immunology 45(14):3723-3730 DOI 10.1016/j.molimm.2008.06.002.
53. Masso-Silva JA, Diamond G. 2014. Antimicrobial peptides from fish. Pharmaceuticals 7(3):265-310 DOI 10.3390/ph7030265.
54. Murphy K, Travers P, Walport M. 2007. Janeway's immunobiology. 7th edition. New York: Garland Science.
55. Murrell B, Moola S, Mabona A, Weighill T, Sheward D, Kosakovsky Pond SL, Scheffler K. 2013. FUBAR: a fast, unconstrained Bayesian approximation for inferring selection. Molecular Biology and Evolution 30(5):1196-1205 DOI 10.1093/molbev/mst030.
56. Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Kosakovsky Pond SL. 2012. Detecting individual sites subject to episodic diversifying selection. PLoS Genetics 8(7):e1002764 DOI 10.1371/journal.pgen.1002764.
57. Nei M, Hughes AL. 1991. Polymorphism and evolution of the major histocompatibility comples loci in mammals. In: Selander R, Clark A, Whittam T, eds. Evolution at the molecular level. Sunderland: Sinauer Associates, Inc., 222-247, chapter 11.
58. Nielsen R, Hellmann I, Hubisz M, Bustamante C, Clark AG. 2007. Recent and ongoing selection in the human genome. Nature Review Genetics 8:857-868 DOI 10.1038/nrg2187.
59. Osborne A, Zavodna M, Chilvers B, Robertson B, Negro S, Kennedy M, Gemmell N. 2013. Extensive variation at MHC DRB in the New Zealand sea lion (Phocarctos hookeri) provides evidence for balancing selection. Heredity 111:44-56 DOI 10.1038/hdy.2013.18.
60. Paradis E. 2010. Pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26:419-420 DOI 10.1093/bioinformatics/btp696.
61. Paradis E, Claude J, Strimmer K. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289-290 DOI 10.1093/bioinformatics/btg412.
62. Pilström L, Warr GW, Strömberg S. 2005. Why is the antibody response of Atlantic cod so poor? The search for a genetic explanation. Fish Science 71:961-971 DOI 10.1111/j.1444-2906.2005.01052.x.
63. Pogson GH. 2001. Nucleotide polymorphism and natural selection at the Pantophysin (Pan I) locus in the Atlantic cod, Gadus morhua (L.). Genetics 157:317-330.
64. Pogson GH, Mesa KA. 2004. Positive Darwinian selection at the Pantophysin (Pan I) locus in marine gadid fishes. Molecular Biology and Evolution 21(1):65-75 DOI 10.1093/molbev/msg237.
65. Pond SLK, Frost SDW, Muse SV. 2005. HyPhy: hypothesis testing using phylogenies. Bioinformatics 21(5):676-679 DOI 10.1093/bioinformatics/bti079.
66. Quintana-Murci L, Clark AG. 2013. Population genetic tools for dissecting innate immunity in humans. Nature Review Immunology 13:280-293 DOI 10.1038/nri3421.
67. R Core Team. 2014. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.
68. Rakers S, Niklasson L, Steinhagen D, Kruse C, Schauber J, Sundell K, Paus R. 2013. Antimicrobial peptides (AMPs) from fish epidermis: perspectives for investigative dermatology. Journal of Investigative Dermatology 133:1140-1149 DOI 10.1038/jid.2012.503.
69. Ruangsri J, Kitani Y, Kiron V, Lokesh J, Brinchmann MF, Karlsen BO, Fernandes JMO. 2013. A novel beta-defensin antimicrobial peptide in Atlantic cod with stimulatory effect on phagocytic activity. PLoS ONE 8(4):e62302 DOI 10.1371/journal.pone.0062302.
70. Shen J, Araki H, Chen L, Chen J-Q, Tian D. 2006. Unique evolutionary mechanism in R-genes under the presence/absence polymorphism in Arabidopsis thaliana. Genetics 172(2):1243-1250 DOI 10.1534/genetics.105.047290.
71. Shin J-H, Blay S, McNeney B, Graham J. 2006. LDheatmap: an R function for graphical display of pairwise linkage disequilibria between single nucleotide polymorphisms. Journal of Statistical Software 16:1-9 Code Snippet 3.
72. Sommer S. 2005. The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Frontiers in Zoology 2(1):16 DOI 10.1186/1742-9994-2-16.
73. Spurgin LG, Richardson DS. 2010. How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proceedings of the Royal Society, B 277(1684):979-988 DOI 10.1098/rspb.2009.2084.
74. Star B, Jentoft S. 2012. Why does the immune system of Atlantic cod lack MHC II? BioEssays 34(8):648-651 DOI 10.1002/bies.201200005.
75. Star B, Nederbragt AJ, Jentoft S, Grimholt U, Malmstrom M, Gregers TF, Rounge TB, Paulsen J, Solbakken MH, Sharma A, Wetten OF, Lanzen A, Winer R, Knight J, Vogel J-H, Aken B, Andersen O, Lagesen K, Tooming-Klunderud A, Edvardsen RB, Tina KG, Espelund M, Nepal C, Previti C, Karlsen BO, Moum T, Skage M, Berg PR, Gjoen T, Kuhl H, Thorsen J, Malde K, Reinhardt R, Du L, Johansen SD, Searle S, Lien S, Nilsen F, Jonassen I, Omholt SW, Stenseth NC, Jakobsen KS. 2011. The genome sequence of Atlantic cod reveals a unique immune system. Nature 477:207-210 DOI 10.1038/nature10342.
76. Sundaram A, Kiron V, Dopazo J, Fernandes J. 2012. Diversification of the expanded teleost-specific toll-like receptor family in Atlantic cod, Gadus morhua. BMC Evolutionary Biology 12(1):256 DOI 10.1186/1471-2148-12-256.
77. Teixeira JC, de Filippo C, Weihmann A, Meneu JR, Racimo F, Dannemann M, Nickel B, Fischer A, Halbwax M, Andre C, Atencia R, Meyer M, Parra G, Pääbo S, Andrés AM. 2014. Long-term balancing selection in LAD1 maintains a missense trans-species polymorphism in humans, chimpanzees and bonobos. bioRxiv Preprint. Available at http://biorxiv.org/content/ biorxiv/early/2014/06/27/006684.full.pdf.
78. Tomasinsig L, Zanetti M. 2005. The cathelicidins-structure, function and evolution. Current Protein and Peptide Science 6:23-34 DOI 10.2174/1389203053027520.
79. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG. 2012. Primer3-new capabilities and interfaces. Nucleic Acids Research 40(15):e115-e115 DOI 10.1093/nar/gks596.
80. Uzzell T, Stolzenberg ED, Shinnar AE, Zasloff M. 2003. Hagfish intestinal antimicrobial peptides are ancient cathelicidins. Peptides 24(11):1655-1667 DOI 10.1016/j.peptides.2003.08.024.
81. Walsh PS, Metzger DA, Higuchi R. 1991. Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques 10:506-513.
82. Wickham H. 2009. ggplot2: elegant graphics for data analysis. New York: Springer.
83. Wiuf C, Zhao K, Innan H, Nordborg M. 2004. The probability and chromosomal extent of trans-specific polymorphism. Genetics 168(4):2363-2372 DOI 10.1534/genetics.104.029488.
84. Yu G. 2015. ggtree: an r package for versatile annotation and visualization of phylogenetic tree. Available at http://github.com/GuangchuangYu/ggtree (accessed 16 April 2015).
85. Zanetti M, Gennaro R, Romeo D. 1995. Cathelicidins: a novel protein family with a common proregion and a variable C-terminal antimicrobial domain. FEBS Letters 374(1):1-5 DOI 10.1016/0014-5793(95)01050-O.
86. Zelezetsky I, Pontillo A, Puzzi L, Antcheva N, Segat L, Pacor S, Crovella S, Tossi A. 2006. Evolution of the primate cathelicidin: Correlation between structural variations and antimicrobial activity. Journal of Biological Chemistry 281(29):19861-19871 DOI 10.1074/jbc.M511108200.
87. Zhang L, Yu J, Wong CCM, Ling TKW, Li ZJ, Chan KM, Ren SX, Shen J, Chan RLY, Lee CC, Li MSM, Cheng ASL, To KF, Gallo RL, Sung JJY, Wu WKK, Cho CH. 2012. Cathelicidin protects against Helicobacter pylori colonization and the associated gastritis in mice. Gene Therapy 20(7):751-760 DOI 10.1038/gt.2012.92.
88. Zhu S. 2008. Positive selection targeting the cathelin-like domain of the antimicrobial cathelicidin family. Cellular and Molecular Life Sciences 65(7-8):1285-1294 DOI 10.1007/s00018-008-8070-x.
89. Zhu S, Gao B. 2009. A fossil antibacterial peptide gives clues to structural diversity of cathelicidin-derived host defense peptides. The FASEB Journal 23(1):13-20 DOI 10.1096/fj.08-114579.
90. Zhuang X, Yang C, Fevolden S-E, Cheng C-H. 2012. Protein genes in repetitive sequence-antifreeze glycoproteins in Atlantic cod genome. BMC Genomics 13(1):293 DOI 10.1186/1471-2164-13-293.