Screening of differentially expressed immune-related genes from spleen of broilers fed with probiotic Bacillus cereus PAS38 based on suppression subtractive hybridization


Autoři: Jiajun Li aff001;  Wanqiang Li aff001;  Jianzhen Li aff001;  Zhenhua Wang aff002;  Dan Xiao aff001;  Yufei Wang aff001;  Xueqin Ni aff001;  Dong Zeng aff001;  Dongmei Zhang aff001;  Bo Jing aff001;  Lei Liu aff001;  Qihui Luo aff001;  Kangcheng Pan aff001
Působiště autorů: College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan Province, China aff001;  Branch of Animal Husbandry and Veterinary Medicine, Chengdu Vocational College of Agricultural Science and Technology, Chengdu, Sichuan Province, China aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226829

Souhrn

The aim of this study was to construct the spleen differential genes library of broilers fed with probiotic Bacillus cereus PAS38 by suppression subtractive hybridization (SSH) and screen the immune-related genes. Sixty seven-day-old broilers were randomly divided into two groups. The control group was fed with basal diet, and the treated group was fed with basal diet containing Bacillus cereus PAS38 1×106 CFU/g. Spleen tissues were taken and extracted its total RNA at 42 days old, then SSH was used to construct differential gene library and screen immune-related genes. A total of 119 differentially expressed sequence tags (ESTs) were isolated by SSH and 9 immune-related genes were screened out by Gene ontology analysis. Nine differentially expressed genes were identified by qRT-PCR. JCHAIN, FTH1, P2RX7, TLR7, IGF1R, SMAD7, and SLC7A6 were found to be significantly up-regulated in the treated group. Which was consistent with the results of SSH. These findings imply that probiotic Bacillus cereus PAS38-induced differentially expressed genes in spleen might play an important role in the improvement of immunity for broilers, which provided useful information for further understanding of the molecular mechanism of probiotics responsible to affect the poultry immunity.

Klíčová slova:

Bacillus cereus – Gene expression – Genetic screens – Chickens – Polymerase chain reaction – Probiotics – Spleen – Toll-like receptors


Zdroje

1. Juan DL, Velasco XH, Wolfenden RE, Vicente JL, Wolfenden AD, Menconi A, et al. Evaluation and selection of Bacillus species based on enzyme production, antimicrobial activity, and biofilm synthesis as direct-fed microbial candidates for poultry. Front Vet Sci. 2016; 3(95):1–9. https://doi.org/10.3389/fvets.2016.00095 27812526

2. Narayanan G, Baskaralingam V, Jiann CC, Rekha R, Vijayakumar S, Anjμgam M, et al. Dietary supplementation of probiotic Bacillus licheniformis Dahb1 improves growth performance, mucus and serum immune parameters, antioxidant enzyme activity as well as resistance against Aeromonas hydrophila in tilapia Oreochromis mossambicus. Fish Shellfish Immunol. 2018; 74: 501–508. https://doi.org/10.1016/j.fsi.2017.12.066 29305993

3. Sikandar A, Zaneb H, Younus M, Masood S, Aslam A, Shah M, et al. Growth performance, immunestatus and organ morphometry in broilers fed Bacillus subtilis-supplemented diet. S Afr J Anim Sci. 2017; 47(3):378–388. https://doi.org/10.4314/sajas.v47i3.14

4. Rajput IR, Ying H, Yajing S, Arain MA, Fen LW, Ping L, et al. Saccharomyces boulardii and Bacillus subtilis B10 modulate TLRs and cytokines expression patterns in jejunum and ileum of broilers. PLoS ONE. 2017; 12(6):e0180752. https://doi.org/10.1371/journal.pone.0180752 28662205

5. Li WF, Jing W, Zhao WH, Ling Z, You YD. Effects of Bacillus Subtilis on growth performance, antioxidant capacity and immunity of intestinal mucosa in broilers. Chin J Anim Sci. 2011; 47(9): 58–61.

6. Gadde U, Oh ST, Lee YS, Davis E, Zimmerman N, Rehberger T, et al. The effects of direct-fed microbial supplementation, as an alternative to antibiotics, on growth performance, intestinal immune status, and epithelial barrier gene expression in broiler chickens. Probiotics Antimicrob Proteins. 2017; 9:397–405. https://doi.org/10.1007/s12602-017-9275-9 28421423

7. Zhao YC, Yuan L, Wan JL, Sun ZX, Wang YY, Sun HS. Effects of potential probiotic Bacillus cereus EN25 on growth, immunity and disease resistance of juvenile sea cucumber Apostichopus japonicas. Fish Shellfish Immunol. 2016; 49:237–242. https://doi.org/10.1016/j.fsi.2015.12.035 26723266

8. Simon MC. Bacillus probiotics. Food Microbiol. 2011; 28(2):214–220. https://doi.org/10.1016/j.fm.2010.03.007 21315976

9. Scharek L, Altherr BJ, Tölke C, Schmidt MFG. Influence of the probiotic Bacillus cereus var. toyoi on the intestinal immunity of piglets. Vet Immunol Immunopathol. 2007; 120(3–4):136–147. https://doi.org/10.1016/j.vetimm.2007.07.015 17870185

10. Pan KC, Chen ZL, Cui HM, Yuan CF, Chen G. Effects of Bacillus cereus PAS38 and mannan preparation on SS and 5-HT immunoreactive cells in small intestine of rabbits. J Zhejiang Univ Sci B. 2009; 35(5):578–584. https://doi.org/10.3785/j.issn.1008-9209.2009.05.016

11. Zhang JC, Yu JF, Hong HL, Liu JC, Lu HL, Yan CL. Identification of heavy metal pollutant tolerance-associated genes in Avicennia marina (Forsk.) by suppression subtractive hybridization. Mar Pollut Bull. 2017; 119(1):81–91. https://doi.org/10.1016/j.marpolbμL.2017.03.023 28343634

12. Gu XX, Zhang J, Wang ZH, Pan KC. Advances in research on Suppressive Subtractive Hybridization (SSH) in animal immune related genes. Chin J Prev Vet Med. 2018; 40(3):269–274. https://doi.org/10.3969/j.issn.1008-0589.201702030

13. Kang XL, Liu YF, Zhang J., Xu QQ, Liu CK, Fang M. Characteristics and expression profile of KRT71 screened by Suppression Subtractive Hybridization cDNA Library in curly fleece Chinese Tan sheep. DNA Cell Biol. 2017; 36(7):1–13. https://doi.org/10.1089/dna.2017.3718 28509589

14. Zhang WW, Jia YF, Wang F, Du QY, Chang ZJ. Identification of differentially-expressed genes in early developmental ovary of Yellow River carp (Cyprinus carpio var) using Suppression Subtractive Hybridization. Theriogenology. 2017; 97(15): 9–16. https://doi.org/10.1016/j.theriogenology.2017.04.017 28583615

15. Gao L, Yang Y, Yao Q, Chen K. Differentially expressed genes in the midguts of BmNPV-susceptible and resistant silkworm strains determined using suppression subtractive hybridization. Invertebrate. Surviv J. 2018; 15:256–264.

16. Xiao Y, An TQ, Tian ZJ, Wei TC, Jiang YF, Peng JM, et al. The gene expression profile of porcine alveolar macrophages infected with a highly pathogenic porcine reproductive and respiratory syndrome virus indicates overstimulation of the innate immune system by the virus. Arch Virol Suppl. 2015; 160, 649–662. https://doi.org/10.1007/s00705-014-2309-7 25504361

17. Brandtzaeg P, Prydz H. Direct evidence for an integrated function of J chain and secretory component in epithelial transport of immunoglobulins. Nature. 1984; 311:71–73. https://doi.org/10.1038/311071a0 6433206

18. Luca T, 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(8):e70650. https://doi.org/10.1371/journal.pone.0070650 23967082

19. Kobayashi K, Hirai H. Studies on subunit components of chicken polymeric immunoglobulins. J Immunol. 1980; 124(4):1695–1704. 6154078

20. Takahashi T, Iwase T, Tachibana T, Komiyama K, Kobayashi K, Chen CL, et al. Cloning and expression of the chicken immunoglobulin joining (J)-chain cDNA. Immunogenetics. 2000; 51:85–91. https://doi.org/10.1007/s002510050016 10663570

21. Nikolov PK, Baleva MP. Alteration of secretory IgA in human breast milk and stool samples after the intake of a probiotic–report of 2 cases. Cent Eur J Med. 2012; 7(1):25–29. https://doi.org/10.2478/s11536-011-0104-3

22. Sarah B, Paubelle E, Bérard E, Thomas ESX, Tavitian S, Larcher MV, et al. Ferritin heavy/light chain (FTH1/FTL) expression, serum ferritin levels and their functional as well as prognostic roles in acute myeloid leukemia. Eur J Haematol. 2019; 102(2):131–142. https://doi.org/10.1111/ejh.13183 30325535

23. Huang HM, Qiu YY, Huang GL, Zhou XH, Zhou XY, Luo WQ. Value of Ferritin Heavy Chain (FTH1) Expression in Diagnosis and Prognosis of Renal Cell Carcinoma. Med Sci Monit. 2019; 25:3700–3715. https://doi.org/10.12659/MSM.914162 31104064

24. Willson NL, Forder REA, Tearle R, Williams JL, Hughes RJ, Nattrass GS, et al. Transcriptional analysis of liver from chickens with fast (meat bird), moderate (F1 layer x meat bird cross) and low (layer bird) growth potential. BMC Genomics. 2018; 19(1): 309. https://doi.org/10.1186/s12864-018-4723-9 29716547

25. Yang KT, Lin CY, Huang HL, Liou JS, Chien CY, Wu CP, et al. Expressed transcripts associated with high rates of egg production in chicken ovarian follicles. Mol Cell Probes. 2008; 22(1):47–54. https://doi.org/10.1016/j.mcp.2007.06.001 17692502

26. Matulova M, Rajova J, Vlasatikova L, Volf J, Stepanova H, Havlickova H, et al. Characterization of Chicken Spleen Transcriptome after Infection with Salmonella enterica Serovar Enteritidis. PLoS One. 2012; 7(10):e48101. https://doi.org/10.1371/journal.pone.0048101 23094107

27. Don NT, Abdul-Careem MF, Shack LA, Burgess SC, Sharif S. Analyses of the spleen proteome of chickens infected with Marek’s disease virus. Virology. 2009; 390(2):356–367. https://doi.org/10.1016/j.virol.2009.05.020 19540544

28. Zhang Y, Tong YY, Chen Y, Huang Z., Zhu Z, Zhang Y, et al. The cSNP scanning and expression analysis of the duck FTH1 gene. Turk J Vet Anim Sci. 2017; 41:12–17. https://doi.org/10.3906/vet-1512-67

29. Su ZH, Wei DJ, Juan L, Meng XC, Xia HY. Role of FTH1 in Brucella infection of host cells. J. Shihezi Univer. (Nat. Sci.). 2014; 32(2):158–163. https://doi.org/10.3969/j.issn.1007-7383.2014.02.006

30. Silva HBD, Wang HG, Qian LJ, Hogquist KA, Jameson SC. ARTC2.2/P2RX7 signaling during cell isolation distorts function and quantification of tissue-resident CD8+ T cell and invariant NKT subsets. J Immunol. 2019; 202(6):1–11. https://doi.org/10.4049/jimmunol.1801613 30777922

31. Pelegrin P, Surprenant A. Pannexin-1 mediates large pore formation and interleukin-1β release by the ATP-gated P2X7 receptor. EMBO J. 2006; 25(21):5071–5082. https://doi.org/10.1038/sj.emboj.7601378 17036048

32. Zhang H, Mehmood K, Jiang X, Yao W, Iqbal M, Li K, et al. Effect of Icariin on Tibial Dyschondroplasia Incidence and Tibial Characteristics by Regulating P2RX7 in Chickens. Biomed Res Int. 2018; 2018:6796271. https://doi.org/10.1155/2018/6796271 29750168

33. Chen Y, Yin Y, Zhen L, Yan HH, Yao GQ. Correlation between P2RX7 gene polymorphism and primary gout in Chinese Han males. Chin J Allergy Clinic Immunol. 2016; 10(4):340–345. https://doi.org/10.3969/j.issn.1673-8705.2016.04.005

34. Ren GC, Wang H, Huang MR, Yan Y, Liu F, Chen R. Transcriptome analysis of fowl adenovirus serotype 4 infection in chickens. Virus Genes. 2019; 55(5):619–629. https://doi.org/10.1007/s11262-019-01676-w 31264023

35. Kalenik BM, Sochacka AG, Stachyra A, Pietrzak M, Kopera E, Fogtman A, et al. Transcriptional response to a prime/boost vaccination of chickens with three vaccine variants based on HA DNA and Pichia-produced HA protein. Dev Comp Immunol. 2018; 88:8–18. https://doi.org/10.1016/j.dci.2018.07.001 29986836

36. Shen L, Qian CH, Cao HM, Wang ZR, Luo TX, Liang CL. Upregulation of the solute carrier family 7 genes is indicative of poor prognosis in papillary thyroid carcinoma. World J Surg Oncol. 2018; 16:235. https://doi.org/10.1186/s12957-018-1535-y 30558624

37. Otsuki H, Kimura T, Kosaka T, Yamaga T, Suehiro JI, Sakurai H. MP83-11 Y+LAT2 (SLC7A6) expression in castration resistant prostate cancer. J Urol. 2017; 197(4):e1110. https://doi.org/10.1016/j.juro.2017.02.2579

38. Kaminski NA, Wong EA. Differential mRNA expression of nutrient transporters in male and female chickens. Poult Sci. 2018; 97(1):313–318. https://doi.org/10.3382/ps/pex262 29077893

39. Beisel C, Ziegler S, Zapater GM, Chapel A, Griesbeck M, Hildebrandt H, et al. TLR7-mediated activation of XBP1 correlates with the IFNα production in humans. Cytokine. 2017; 94:55–58. https://doi.org/10.1016/j.cyto.2017.04.006 28408069

40. Gupta SK, Deb R, Dey S, Chellappa MM. Toll-like receptor-based adjuvants: enhancing the immune response to vaccines against infectious diseases of chicken. Expert Review of Vaccines. 2014; 13(7):909–925. https://doi:10.1586/14760584.2014.920236 24855906

41. Xiang B, Zhu W, Li Y, Gao P, Liang J, Liu D, et al. Immune responses of mature chicken bone‑marrow‑derived dendritic cells infected with Newcastle disease virus strains with differing pathogenicity. Arch Virol. 2018; 163(6):1407–1417. https://doi:10.1007/s00705-018-3745-6 29397456

42. Kingma SD, Li N, Sun F, Valladares RB, Neu J, Lorcaet GL. Lactobacillus johnsonii N6.2 stimulates the innate immune response through toll-like receptor 9 in Caco-2 cells and increases intestinal crypt paneth cell number in biobreeding diabetes-prone rats. J Nutr. 2011; 141(6):1023–1028. https://doi.org/10.3945/jn.110.135517 21490291

43. Guo MJ, Hao GG, Wang BH, Li N, Li R, Wei LM, et al. Dietary administration of Bacillus subtilis enhances growth performance, immune response and disease resistance in cherry valley ducks. Front Microbiol. 2016; 7:1–9. https://doi.org/10.3389/fmicb.2016.01975 28008328

44. Wang JF, Lian S, He XJ, Yu DB, Liang JB, Sun DB, et al. Selenium deficiency induces splenic growth retardation by deactivating the IGF-1R/PI3K/Akt/mTOR pathway. Metallomics. 2018; 11: 1570–1575. https://doi.org/10.1039/c8mt00183a 30349927

45. Wu PF, Wang D, Jin CF, Zhang XQ, Wu HQ, Zhang L, et al. Polymorphisms of Alul and Hin1I loci of the IGF-1R gene and their genetic effects on growth traits in Bian chickens. Genet. Mol. Res. 2017; 16(2):gmr16029619. https://doi.org/10.4238/gmr16029619 28437555

46. Alzaid A, Martin SAM, Macqueen DJ. The complete salmonid IGF-IR gene repertoire and its transcriptional response to disease. Sci Rep. 2016; 6:34806. https://doi.org/10.1038/srep34806 27748369

47. Gioacchini G, Elia C, Andrea P, Cinzia C, Stefania S, Ana R, et al. Effects of lactogen 13, a new probiotic preparation, on gut microbiota and endocrine signals controlling growth and appetite of Oreochromis niloticus juveniles. Microb Ecol. 2018; 76(4):1063–1074. https://doi.org/10.1007/s00248-018-1177-1 29616281

48. Katsuno Y, Qin J, Prieto JO, Wang HJ, Weaver OJ, Zhang TW, et al. Arginine methylation of SMAD7 by PRMT1 in TGF-β–induced epithelial–mesenchymal transition and epithelial stem-cell generation. J Biol Chem. 2018; 293:13059–13072. https://doi.org/10.1074/jbc.RA118.002027 29907569

49. Yan XH, Liu ZY, Chen YG. RegμLation of TGF-β signaling by Smad7. Acta Biochim Biophys Sin. 2009; 41(4):263–272. https://doi.org/10.1016/j.cpc.2007.09.008 19352540

50. Lukas D, Yogev N, Kel JM, Regen T, Mufazalov IA, Tang Y, et al. TGF-β inhibitor Smad7 regμLates dendritic cell-induced autoimmunity. Proc Natl Acad Sci. 2017; 114(8):E1480–E1489. https://doi.org/10.1073/pnas.1615065114 28167776

51. Zuo QS, Jin K, Zhang YN, Song JZ, Li BC. Dynamic expression and regulatory mechanism of TGF-β signaling in chicken embryonic stem cells differentiating into spermatogonial stem cells. Biosci Rep. 2017; 37(4):BSR20170179. https://doi.org/10.1042/BSR20170179 28495881

52. Khatri B, Seo D, Shouse S, Pan JH, Hudson NJ, Kim JK, et al. MicroRNA profiling associated with muscle growth in modern broilers compared to an unselected chicken breed. BMC Genomics. 2018; 19:683. https://doi.org/10.1186/s12864-018-5061-7 30223794

53. Fujii T, Yoshikazu O, Tsubasa L, Takahiro K, Hiromichi S, Hiroaki S, et al. Bifidobacterium breve enhances transforming growth factor β1 signaling by regulating smad7 expression in preterm infants. J Pediatr Gastroenterol Nutr. 2006; 43(1):83–88. https://doi.org/10.1097/01.mpg.0000228100.04702.f8 16819382

54. Darzi L, Boshtam M, Shariati L, Kouhpayeh S, Gheibi A, Mirian M, et al. The silencing effect of miR-30a on ITGA4 gene expression in vitro: an approach for gene therapy. Res Pharm Sci. 2017; 12(6):456–464. https://doi.org/10.4103/1735-5362.217426 29204174

55. Woyciechowski S, Hofmann M, Pircher H. α4β1 integrin promotes accumulation of tissue‐resident memory CD8+ T cells in salivary glands. Eur J Immunol. 2017; 47:244–250. https://doi.org/10.1002/eji.201646722 27861803

56. Kim CH, Lillehoj HS, Hong YH, Keeler CL, Lillehoj EP. Comparison of global transcriptional responses to primary and secondary Eimeria acervulina infections in chickens. Dev Comp Immunol. 2010; 34(3):344–351. https://doi.org/10.1016/j.dci.2009.11.006 19941894

57. Heidari M, Wang D, Sun SH. Early Immune Responses to Marek’s Disease Vaccines. Viral Immunol. 2017; 30(3):167–177. https://doi.org/10.1089/vim.2016.0126 28346793

58. Segal L, Etzion S, Elyagon S, Numa M, Livitas A, Muhammad E, et al. DOCK10 is vital for normal cardiac function under neurohormonal activation. J Mol Cell Cardiol. 2018; 120:18. https://doi.org/10.1016/j.yjmcc.2018.05.061

59. Yelo E, Bernardo MV, Gimeno L, García MJA, Majado MJ, Parradoa A. Dock10, a novel CZH protein selectively induced by interleukin-4 in human B lymphocytes. Mol Immunol. 2008; 45(12): 3411–3418. https://doi.org/10.1016/j.molimm.2008.04.003 18499258

60. Serna AMG, García MJA, Lafuente NR, Ruiz SS, Martínez CM, Quiles MRM, et al. Dock10 regulates CD23 expression and sustains B-cell lymphopoiesis in secondary lymphoid tissue. Immunobiology. 2016; 221(12):1343–1350. https://doi.org/10.1016/j.imbio.2016.07.015 27502165

61. Gerasimčik N, He MH, Baptista MAP, Severinson E, Westerberg LS. Deletion of dock10 in B cells results in normal development but a mild deficiency upon in vivo and in vitro stimulations. Front Immunol. 2017; 8(491):1–15. https://doi.org/10.3389/fimmu.2017.00491 28507547

62. Monson MS, Settlage RE, Mendoza KM, Rawal S, El-Nezami HS, Coulombe RA. Modulation of the spleen transcriptome in domestic turkey (Meleagris gallopavo) in response to aflatoxin B1 and probiotics. Immunogenetics. 2015; 67(3):163–178. https://doi.org/10.1007/s00251-014-0825-y 25597949

63. Ansari AR, Li NY, Sun ZJ, Huang HB, Zhao X, Cui L, et al. Lipopolysaccharide induces acute bursal atrophy in broiler chicks by activating TLR4-MAPK-NF-κB/AP-1 signaling. Oncotarget. 2017; 8(65):108375–108391. https://doi.org/10.18632/oncotarget.19964 29312537

64. Isolauri E, Sütas Y, Kankaanpää P, Arvilommi H, Salminen S. Probiotics: effects on immunity. Am J Clin Nutr. 2001; 73(2):444–450. https://doi.org/10.1093/ajcn/73.2.444s 11157355

65. Daisuke T, Kurashima Y, Kamioka M, Nakayama T, Ernst P, Kiyono H. A comprehensive understanding of the gut mucosal immune system in allergic inflammation. Allergol Int. 2019; 9(4): 1–9. https://doi.org/10.1016/j.alit.2018.09.004 30366757


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