Effect on the splenocyte function of weaned piglets induced by continuous lipopolysaccharide injections

Tingyu Yang; Guotong Zhao; Wenlu Zhu; Wanting Yu; Yijie Jiang; Yunxiao Zhou; Yong Li

doi:10.2478/jvetres-2024-0024

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Effect on the splenocyte function of weaned piglets induced by continuous lipopolysaccharide injections

Journal of Veterinary Research

Volume 68 (2024): Issue 2 (June 2024)

By: Tingyu Yang , Guotong Zhao , Wenlu Zhu , Wanting Yu , Yijie Jiang , Yunxiao Zhou and Yong Li

Open Access

|May 2024

Abstract

Introduction

When piglets are exposed to pathogens for a long period, the immune system organs, among them the spleen, play a major role in combating the stress caused by those pathogens. In the present study, the effect on splenocyte function was investigated in a model of weaned piglets in which stress was induced by multiple low doses of lipopolysaccharide (LPS).

Material and Methods

Forty-eight 28-day-old piglets were divided into two groups: the LPS group and the control group. During the experimental period of thirteen days, the LPS group was intraperitoneally injected with LPS (100 μg/kg) once per day, and the control group was injected with the same volume of 0.9% sterile saline. On the 1^st, 5^th, 9^th and 13^th days, the piglets’ spleens were collected for isolating splenocytes. The proliferation ability of splenocytes was evaluated by the cell-counting-kit 8 method. Flow cytometry was used to detect cell cycle stage and apoptosis, and the nitric oxide level of cell supernatant was also tested.

Results

In the experimental group, the proliferation ability of splenocytes was enhanced, the proportion of cells in the G0/G1 phase was smaller, and cells were promoted to the S and G2/M phases. Meanwhile, apoptosis was suppressed and nitric oxide release upregulated. The results were significantly different between the LPS group and the control group on the 5^th and 9^th days.

Conclusion

The difference between the results of one group and those of the other suggest that after the 5^th LPS injection, multiple low doses of LPS activated splenocytes and restored the number of splenocytes, which maintained and possibly enhanced the regulation of the immune function of the spleen.

References

Basile F., Capaccia C., Zampini D., Biagetti T., Diverio S., Guelfi G.: Omics insights into animal resilience and stress factors. Animals 2021, 11, 47, doi: 10.3390/ani11010047.
Open DOI Search in Google Scholar Back to article
Baumann S., Krueger A., Kirchhoff S., Krammer P.: Regulation of T cell apoptosis during the immune response. Curr Mol Med 2002, 2, 257–272, doi: 10.2174/1566524024605671.
Open DOI Search in Google Scholar Back to article
Bogdan C.: Nitric oxide and the immune response. Nat Immunol 2001, 2, 907–916, doi: 10.1038/ni1001-907.
Open DOI Search in Google Scholar Back to article
Collier R.J., Baumgard L.H., Zimbelman R.B., Xiao Y.: Heat stress: physiology of acclimation and adaptation. Anim Front 2019, 9, 12–19, doi: 10.1093/af/vfy031.
Open DOI Search in Google Scholar Back to article
Connelly L., Palacios-Callender M., Ameixa C., Moncada S., Hobbs A.J.: Biphasic regulation of NF-kappa B activity underlies the pro- and anti-inflammatory actions of nitric oxide. J Immunol 2001, 166, 3873–3881, doi: 10.4049/jimmunol.166.6.3873.
Open DOI Search in Google Scholar Back to article
Crane G.M., Liu Y.C., Chadburn A.: Spleen: development, anatomy and reactive lymphoid proliferations. Semin Diagn Pathol 2021, 38, 112–124, doi: 10.1053/j.semdp.2020.06.003.
Open DOI Search in Google Scholar Back to article
Dhabhar F.S., Saul A.N., Daugherty C., Holmes T.H., Bouley D.M., Oberyszyn T.M.: Short-term stress enhances cellular immunity and increases early resistance to squamous cell carcinoma. Brain Behav Immun 2010, 24, 127–137, doi: 10.1016/j.bbi.2009.09.004.
Open DOI Search in Google Scholar Back to article
Dwijayanti D.R., Djati M.S., Rifa I.M.: The role of VipAlbumin® as an immunostimulatory agent for controlling homeostasis and proliferation of lymphoid cells. Cent Eur J Immunol 2016, 41, 31–38, doi: 10.5114/ceji.2016.58814.
Open DOI Search in Google Scholar Back to article
Fan W., Zheng P., Wang Y., Hao P., Liu J., Zhao X.: Analysis of immunostimulatory activity of polysaccharide extracted from Yu-Ping-Feng in vitro and in vivo. Biomed Pharmacother 2017, 93, 146–155, doi: 10.1016/j.biopha.2017.05.138.
Open DOI Search in Google Scholar Back to article
Fang J., Zhu P., Yang Z., Peng X., Zuo Z., Cui H., Ouyang P., Shu G., Chen Z., Huang C., Liu W.: Selenium ameliorates AFB1-induced excess apoptosis in chicken splenocytes through death receptor and endoplasmic reticulum pathways. Biol Trace Elem Res 2019, 187, 273–280, doi: 10.1007/s12011-018-1361-7.
Open DOI Search in Google Scholar Back to article
He Y., Mo Q., Hu Y., Chen W., Luo B., Wu L., Qiao Y., Xu R., Zhou Y., Zuo Z., Deng J., He W., Wei Y.: E. adenophorum induces cell cycle arrest and apoptosis of splenocytes through the mitochondrial pathway and caspase activation in Saanen goats. Sci Rep 2015, 5, 15967, doi: 10.1038/srep15967.
Open DOI Search in Google Scholar Back to article
Hong Y., Lee J., Vu T.H., Lee S., Lillehoj H.S., Hong Y.H.: Exosomes of lipopolysaccharide-stimulated chicken macrophages modulate immune response through the MyD88/NF-kappaB signaling pathway. Dev Comp Immunol 2021, 115, 103908, doi: 10.1016/j.dci.2020.103908.
Open DOI Search in Google Scholar Back to article
Hou Y., Yao K., Wang L., Ding B., Fu D., Liu Y., Zhu H., Liu J., Li Y., Kang P., Yin Y., Wu G.: Effects of α-ketoglutarate on energy status in the intestinal mucosa of weaned piglets chronically challenged with lipopolysaccharide. Br J Nutr 2011, 106, 357–363, doi: 10.1017/S0007114511000249.
Open DOI Search in Google Scholar Back to article
Jafari-Khataylou Y., Emami S.J., Mirzakhani N.: Troxerutin attenuates inflammatory response in lipopolysaccharide-induced sepsis in mice. Res Vet Sci 2021, 135, 469–478, doi: 10.1016/j.rvsc.2020.11.020.
Open DOI Search in Google Scholar Back to article
Kim H.B., Lee H.S., Kim S.J., Yoo H.J., Hwang J.S., Chen G., Youn H.J.: Ethanol extract of fermented soybean, Chungkookjang, inhibits the apoptosis of mouse spleen, and thymus cells. J Microbiol 2007, 45, 256–261.
Search in Google Scholar Back to article
Kudryavtseva N.N., Shurlygina A.V., Melnikova E.V., Tenditnik M.V., Bondar N.P., Panteleeva N.G., Smagin D.A., Kolesnikov N.N., Trufakin V.A.: Cell cycle arrest in the thymus and spleen in male mice under conditions of chronic social defeat stress: effects of diazepam. Bull Exp Biol Med 2011, 151, 411–414, doi: 10.1007/s10517-011-1343-7.
Open DOI Search in Google Scholar Back to article
Laukova M., Vargovic P., Rokytova I., Manz G., Kvetnansky R.: Repeated stress exaggerates lipopolysaccharide-induced inflammatory response in the rat spleen. Cell Mol Neurobiol 2018, 38, 195–208, doi: 10.1007/s10571-017-0546-5.
Open DOI Search in Google Scholar Back to article
Li T., Shi H.Y., Hua Y.X., Gao C., Xia Q., Yang G., Li B.: Effects of allicin on the proliferation and cell cycle of chondrocytes. Int J Clin Exp Pathol 2015, 8, 12525–12532.
Search in Google Scholar Back to article
Lin P., Ding B., Wu Y., Dong K., Li Q.: Mitogen-stimulated cell proliferation and cytokine production in major depressive disorder patients. BMC Psychiatry 2018, 18, 330, doi: 10.1186/s12888-018-1906-5.
Open DOI Search in Google Scholar Back to article
Liu Y.L., Li D.F., Gong L.M., Yi G.F., Gaines A.M., Carroll J.A.: Effects of fish oil supplementation on the performance and the immunological, adrenal, and somatotropic responses of weaned pigs after an Escherichia coli lipopolysaccharide challenge. J Anim Sci 2003, 81, 2758–2765, doi: 10.2527/2003.81112758x.
Open DOI Search in Google Scholar Back to article
Ma T., Kang C., Shao H., Qi Q., Hu W.: Protective effects of ulinastatin on proliferation and cytokine release of splenocytes from rats with severe acute pancreatitis. Eur Surg Res 2006, 38, 445–450, doi: 10.1159/000095087.
Open DOI Search in Google Scholar Back to article
Mao X.F., Piao X.S., Lai C.H., Li D.F., Xing J.J., Shi B.L.: Effects of beta-glucan obtained from the Chinese herb Astragalus membranaceus and lipopolysaccharide challenge on performance, immunological, adrenal, and somatotropic responses of weanling pigs. J Anim Sci 2005, 83, 2775–2782, doi: 10.2527/2005.83122775x.
Open DOI Search in Google Scholar Back to article
Martinez-Miro S., Tecles F., Ramon M., Escribano D., Hernandez F., Madrid J., Orengo J., Martinez-Subiela S., Manteca X., Ceron J.J.: Causes, consequences and biomarkers of stress in swine: an update. BMC Vet Res 2016, 12, 171, doi: 10.1186/s12917-016-0791-8.
Open DOI Search in Google Scholar Back to article
Michalek R.D., Rathmell J.C.: The metabolic life and times of a T-cell. Immunol Rev 2010, 236, 190–202, doi: 10.1111/j.1600-065X.2010.00911.x.
Open DOI Search in Google Scholar Back to article
Mitra S., Keswani T., Dey M., Bhattacharya S., Sarkar S., Goswami S., Ghosh N., Dutta A., Bhattacharyya A.: Copper-induced immunotoxicity involves cell cycle arrest and cell death in the spleen and thymus. Toxicology 2012, 293, 78–88, doi: 10.1016/j.tox.2011.12.013.
Open DOI Search in Google Scholar Back to article
Nagy G., Clark J.M., Buzas E., Gorman C., Pasztoi M., Koncz A., Falus A., Cope A.P.: Nitric oxide production of T lymphocytes is increased in rheumatoid arthritis. Immunol Lett 2008, 118, 55–58, doi: 10.1016/j.imlet.2008.02.009.
Open DOI Search in Google Scholar Back to article
Niedbala W., Wei X.Q., Campbell C., Thomson D., Komai-Koma M., Liew F.Y.: Nitric oxide preferentially induces type 1 T cell differentiation by selectively up-regulating IL-12 receptor beta 2 expression via cGMP. Proc Natl Acad Sci USA 2002, 99, 16186–16191, doi: 10.1073/pnas.252464599.
Open DOI Search in Google Scholar Back to article
Niu X., Ding Y., Chen S., Gooneratne R., Ju X.: Effect of immune stress on growth performance and immune functions of livestock: mechanisms and prevention. Animals 2022, 12, 909, doi: 10.3390/ani12070909.
Open DOI Search in Google Scholar Back to article
Nogueira J.E., Agostinho B.K.L., Mota C.M.D., Branco L.G.S.: Splenic anti-inflammatory reflex in immune tolerance. J Therm Biol 2019, 85, 102411, doi: 10.1016/j.jtherbio.2019.102411.
Open DOI Search in Google Scholar Back to article
Peng X., Cui H., Deng J., Zuo Z., Lai W.: Histological lesion of spleen and inhibition of splenocyte proliferation in broilers fed on diets excess in selenium. Biol Trace Elem Res 2011, 140, 66–72, doi: 10.1007/s12011-010-8679-0.
Open DOI Search in Google Scholar Back to article
Peng X., Zhang K., Bai S., Ding X., Zeng Q., Yang J., Fang J., Chen K.: Histological lesions, cell cycle arrest, apoptosis and T Cell subsets changes of spleen in chicken fed aflatoxin-contaminated corn. Int J Environ Res Public Health 2014, 11, 8567–8580, doi: 10.3390/ijerph110808567.
Open DOI Search in Google Scholar Back to article
Sassi A., Mokdad Bzeouich I., Mustapha N., Maatouk M., Ghedira K., Chekir-Ghedira L.: Immunomodulatory potential of hesperetin and chrysin through the cellular and humoral response. Eur J Pharmacol 2017, 812, 91–96, doi: 10.1016/j.ejphar.2017.07.017.
Open DOI Search in Google Scholar Back to article
Satoh E., Edamatsu H., Omata Y.: Acute restraint stress enhances calcium mobilization and proliferative response in splenic lymphocytes from mice. Stress 2006, 9, 223–230, doi: 10.1080/10253890601095794.
Open DOI Search in Google Scholar Back to article
Shen J., Yu S.F., Peng M., Lai D.H., Hide G., Wu Z.D., Lun Z.R.: iNOS is essential to maintain a protective Th1/Th2 response and the production of cytokines/chemokines against Schistosoma japonicum infection in rats. PLoS Negl Trop Dis 2022, 16, e0010403, doi: 10.1371/journal.pntd.0010403.
Open DOI Search in Google Scholar Back to article
Tanaka H., Nishikawa Y., Fukushima T., Taniguchi A., Fujita Y., Tsuda K., Inagaki N., Hosokawa M.: Lipopolysaccharide inhibits hepatic gluconeogenesis in rats: the role of immune cells. J Diabetes Investig 2018, 9, 494–504, doi: 10.1111/jdi.12729.
Open DOI Search in Google Scholar Back to article
Tang X., Xiong K., Fang R., Li M.: Weaning stress and intestinal health of piglets: a review. Front Immunol 2022, 13, 1042778, doi: 10.3389/fimmu.2022.1042778.
Open DOI Search in Google Scholar Back to article
Terenina E., Sautron V., Ydier C., Bazovkina D., Sevin-Pujol A., Gress L., Lippi Y., Naylies C., Billon Y., Liaubet L., Mormede P., Villa-Vialaneix N.: Time course study of the response to LPS targeting the pig immune gene networks. BMC Genomics 2017, 18, 988, doi: 10.1186/s12864-017-4363-5.
Open DOI Search in Google Scholar Back to article
Wang L., Jing J., Yan H., Tang J., Jia G., Liu G., Chen X., Tian G., Cai J., Shang H., Zhao H.: Selenium pretreatment alleviated LPS-induced immunological stress via upregulation of several selenoprotein encoding genes in murine RAW264.7 cells. Biol Trace Elem Res 2018, 186, 505–513, doi: 10.1007/s12011-018-1333-y.
Open DOI Search in Google Scholar Back to article
Wyns H., Plessers E., De Backer P., Meyer E., Croubels S.: In vivo porcine lipopolysaccharide inflammation models to study immunomodulation of drugs. Vet Immunol Immunopathol 2015, 166, 58–69, doi: 10.1016/j.vetimm.2015.06.001.
Open DOI Search in Google Scholar Back to article
Yu J., Zheng C., Zheng J., Duan G., Guo Q., Zhang P., Wan M., Duan Y.: Development of intestinal injury and restoration of weaned piglets under chronic immune stress. Antioxidants 2022, 11, 2215, doi: 10.3390/antiox11112215.
Open DOI Search in Google Scholar Back to article
Yu Y., Wang H., Meng X., Hao L., Fu Y., Fang L., Shen D., Yu X., Li J.: Immunomodulatory effects of cinobufagin on murine lymphocytes and macrophages. Evid Based Complement Alternat Med 2015, 2015, 835263, doi: 10.1155/2015/835263.
Open DOI Search in Google Scholar Back to article
Zhang X., Xiao K., Qiu W., Wang J., Li P., Peng K.: The immune regulatory effect of boron on ostrich chick splenic lymphocytes. Biol Trace Elem Res 2021, 199, 2695–2706, doi: 10.1007/s12011-020-02392-5.
Open DOI Search in Google Scholar Back to article
Zhou Y., Hu X., Zhong, S., Yu W., Wang J, Zhu W., Yang T., Zhao G., Jiang Y., Li, Y.: Effects of continuous LPS induction on oxidative stress and liver injury in weaned piglets. Vet Sci 2023, 10, 22, doi: 10.3390/vetsci10010022.
Open DOI Search in Google Scholar Back to article

Articles in this issue

DOI: https://doi.org/10.2478/jvetres-2024-0024 | Journal eISSN: 2450-8608

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Language: English

Page range: 295 - 302

Submitted on: Oct 28, 2023

Accepted on: Apr 22, 2024

Published on: May 9, 2024

Published by: National Veterinary Research Institute in Pulawy

In partnership with: Paradigm Publishing Services

Publication frequency: 4 issues per year

Keywords:

LPS,

Related subjects:

Microbiology and virology,

Life sciences, other,

Medicine,

Veterinary medicine

© 2024 Tingyu Yang, Guotong Zhao, Wenlu Zhu, Wanting Yu, Yijie Jiang, Yunxiao Zhou, Yong Li, published by National Veterinary Research Institute in Pulawy
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.

Volume 68 (2024): Issue 2 (June 2024)