Comparative study of four interleukin 17 cytokines of tongue sole Cynoglossus semilaevis: genomic structure, expression pattern, and promoter activityFish & Shellfish Immunology

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Authors
Heng Chi, Li Sun
Year
2015
DOI
10.1016/j.fsi.2015.09.020
Subject
Aquatic Science / Environmental Chemistry

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Accepted Manuscript

Comparative study of four interleukin 17 cytokines of tongue sole Cynoglossus semilaevis: genomic structure, expression pattern, and promoter activity

Heng Chi, Li Sun

PII: S1050-4648(15)30145-5

DOI: 10.1016/j.fsi.2015.09.020

Reference: YFSIM 3608

To appear in: Fish and Shellfish Immunology

Received Date: 28 May 2015

Revised Date: 7 September 2015

Accepted Date: 8 September 2015

Please cite this article as: Chi H, Sun L, Comparative study of four interleukin 17 cytokines of tongue sole Cynoglossus semilaevis: genomic structure, expression pattern, and promoter activity, Fish and

Shellfish Immunology (2015), doi: 10.1016/j.fsi.2015.09.020.

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ACCEPTED MANUSCRIPT 1

Comparative study of four interleukin 17 cytokines of tongue sole 1

Cynoglossus semilaevis: genomic structure, expression pattern, 2 and promoter activity 3 4

Heng Chi, Li Sun* 5 6

Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, 7

Qingdao 266071, China 8

Function Laboratory for Marine Biology and Biotechnology, Qingdao National Oceanography Laboratory, 9

Qingdao, China 10 11 12 *To whom correspondence should be addressed 13 14

Mailing address: 15

Li Sun 16

Institute of Oceanology 17

Chinese Academy of Sciences 18 7 Nanhai Road 19

Qingdao 266071, China 20

Phone: 86-532-82898829 21

Email: lsun@qdio.ac.cn 22 23

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Abstract 24 25

The interleukin (IL)-17 cytokine family participates in the regulation of many cellular functions. In the 26 present study, we analyzed the genomic structure, expression, and promoter activity of four IL-17 members 27 from the teleost fish tongue sole (Cynoglossus semilaevis), i.e. CsIL-17C CsIL-17D, CsIL-17F, and IL-17F 28 like (IL-17Fl). We found that CsIL-17C, CsIL-17D, CsIL-17F, and CsIL-17Fl share 21.2%-28.6% overall 29 sequence identities among themselves and 31.5%-71.2% overall sequence identities with their counterparts 30 in other teleost. All four CsIL-17 members possess an IL-17 domain and four conserved cysteine residues. 31

Phylogenetic analysis classified the four CsIL-17 members into three clusters. Under normal physiological 32 conditions, the four CsIL-17 expressed in multiple tissues, especially non-immune tissues. Bacterial 33 infection upregulated the expression of all four CsIL-17, while viral infection upregulated the expression of 34

CsIL-17D and CsIL-17Fl but downregulated the expression of CsIL-17C and CsIL-17F. The 1.2 kb 35 5’-flanking regions of the four CsIL-17 exhibited apparent promoter activity and contain a number of 36 putative transcription factor-binding sites. Furthermore, the promoter activities of CsIL-17C, CsIL-17D, 37 and CsIL-17F, but not CsIL-17Fl, were modulated to significant extents by lipopolysaccharide, PolyI:C, 38 and PMA. This study provides the first evidence that in teleost, different IL-17 members differ in 39 expression pattern and promoter activity. 40 41

Key words: interleukin 17; Cynoglossus semilaevis; expression pattern; promoter activity 42 43

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ACCEPTED MANUSCRIPT 3 1. Introduction 44 45

Interleukin (IL) is a group of cytokines that were first seen to be expressed by white blood cells. The 46 function of the immune system depends in a large part on interleukins, and rare deficiencies of a number of 47 interleukins have been described, all featuring autoimmune diseases or immune deficiency [1]. The 48 interleukin 17 (IL-17) family, a subset of cytokines consisting of IL-17A (CTLA8), IL-17B, IL-17C, 49

IL-17D, IL-17E ( IL-25), and IL-17F, have been reported to play crucial roles in host defense against 50 microbial organisms and in the development of inflammatory diseases [2]. 51

The IL-17 cytokine family, derived from a wide array of cell types, participates in the regulation of 52 many cellular functions [2]. IL-17A was originally identified as a transcript from a rodent T-cell hybridoma 53 [3]. IL-17A+ T helper cells, also called Th17 cells, play a pathological role in inflammatory and 54 autoimmune diseases [4]. IL-17B and IL-17C differ from IL-17A in their patterns of expression and 55 biological activities, and are unable to interact with the IL-17A receptor [5]. IL-17D is similar to other 56 members of the IL-17 family and thought to indirectly modulate immune response by regulating cytokine 57 production [5]. However, unlike other IL-17 family members, IL-17D is reported to be preferentially 58 expressed in skeletal muscle, brain, adipose tissue, heart and pancreas, thus playing an additional role in 59 local immune responses [6]. Moreover, IL-17D is evolutionarily most conserved IL-17 member [7,8]. 60

IL-17F shares high similarities with IL-17A and is widely recognized as an inflammatory cytokine. The 61 genes encoding IL-17A and IL-17F are localized in the same chromosomal region and co-expressed by 62

CD4+ and γδ T cells in mammals [9]. 63

In teleost, interleukins are known to play important roles in antimicrobial immunity [10-13]. For IL-17, 64 its members have been identified in several fish species [14-20], but little is known about their biological 65

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ACCEPTED MANUSCRIPT 4 function. Recent genomic sequencing reveals the existence of four IL-17 members in tongue sole 66 (Cynoglossus semilaevis) [21], i.e. IL-17C, IL-17D, IL-17F and IL-17F like (IL-17Fl), which were named 67

CsIL-17C, CsIL-17D, CsIL-17F, and CsIL-17Fl respectively in this study. With an aim to gain insight into 68 the function and regulation of teleost IL-17, we in this report analyzed the genomic structure, expression 69 profile, and promoter activity of the four IL-17 members of tongue sole. 70 71 2. Materials and methods 72 73 2.1 Fish 74 75