Developmental Competence of Embryo vis-à-vis Lipopolysaccharide

Authors

  • Sujata Jinagal Animal Physiology and Reproduction Division, ICAR-Central Institute for Research on Buffaloes, Hisar-125001, Haryana, India
  • Ravi Dutt Department of Veterinary Gynaecology and Obstetrics, Lala Lajpat Rai University of Veterinary and Animal Sciences, Hisar, 125004, Haryana, India
  • Swati Thakur Animal Physiology and Reproduction Division, ICAR-Central Institute for Research on Buffaloes, Hisar-125001, Haryana, India
  • Meeti Punetha Animal Physiology and Reproduction Division, ICAR-Central Institute for Research on Buffaloes, Hisar-125001, Haryana, India
  • Maninder Sharma Animal Physiology and Reproduction Division, ICAR-Central Institute for Research on Buffaloes, Hisar-125001, Haryana, India
  • Sheetal Saini Animal Physiology and Reproduction Division, ICAR-Central Institute for Research on Buffaloes, Hisar-125001, Haryana, India
  • Suman Chaudhary Animal Physiology and Reproduction Division, ICAR-Central Institute for Research on Buffaloes, Hisar-125001, Haryana, India
  • Pradeep Kumar Animal Physiology and Reproduction Division, ICAR-Central Institute for Research on Buffaloes, Hisar-125001, Haryana, India
  • P S Yadav Animal Physiology and Reproduction Division, ICAR-Central Institute for Research on Buffaloes, Hisar-125001, Haryana, India
  • Dharmendra Kumar Animal Physiology and Reproduction Division, ICAR-Central Institute for Research on Buffaloes, Hisar-125001, Haryana, India

DOI:

https://doi.org/10.48165/aru.2023.3.1.6

Keywords:

Buffalo, Developmental competence, Embryo, Lipopolysaccharide, Oocytes

Abstract

Post-partum uterine inflammation in dairy bovines impairs the reproductive process  resulting in extended anestrus, reduced conception and increased pregnancy attrition.  Pathogen associated molecular patterns (PAMPs) are a set of molecular motifs that  are present on the surface of various classes of microbes. Bacterial lipopolysaccharides  (LPSs) are an endotoxin found in the cell membranes of Gram-negative bacteria, are  considered as a prototypical class of PAMPs. Among PAMPs, LPS is the most potent  one present on the surface of E. coli associated with endometritis and inflammation of  the uterus. When ovarian follicular cells are exposed to LPS, toll-like receptor (TLR)  and cluster of differentiation 14 (CD14) will be expressed, activating to culminate in  the up-regulation of pro-inflammatory cytokines like IL-1β, IL-18 and TNF which  reacts directly to bacterial products and impairing reproductive functions. Although,  both theca interna and granulosa cells are capable of responding to inflammatory  mediators and altering some functions of the oocytes may result in failure of the oocyte  to become fully competent, even if the insult occurs well before ovulation. Several  studies have been focused on the effect of LPS on the reproductive performance of dairy  animals but the effect of LPS on oocytes during maturation and their development is  yet to be defined well. Therefore, the present review emphasized on the effect of LPS  on important female reproductive functions and possible mechanism of bacterial  endotoxin LPS action on the embryonic development through various pathways. 

References

Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell. 2006;124(4):783-801. doi: 10.1016/j. cell.2006.02.015.

Akira S. Mammalian Toll-like receptors. Curr Opin Immunol. 2003; 15(2):238. doi: 10.1016/s0952-7915(02)00013-4. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA. Recognition of double-stranded RNA and activation of NF-kappaB by

Toll-like receptor 3. Nature. 2001;413(6857):732-8. doi: 10.1038/35099560.

Barlund CS, Carruthers TD, Waldner CL, Palmer CW. A com parison of diagnostic techniques for postpartum endome tritis in dairy cattle. Theriogenology. 2008;69(6):714-23. doi.org/10.1016/j.theriogenology.2007.12.005.

Battaglia DF, Krasa HB, Padmanabhan V, Viguié C, Karsch FJ. Endocrine alterations that underlie endotoxin-induced dis ruption of the follicular phase in ewes. Biol Reprod. 2000; 62(1):45-53. doi: 10.1095/biolreprod62.1.45.

Bidne KL, Dickson MJ, Ross JW, Baumgard LH, Keating AF. Disruption of female reproductive function by endotoxins. Reproduction. 2018;155(4): R169-81. doi: 10.1530/REP-17- 0406.

Biscari L, Kaufman CD, Farré C, Huhn V, Pacini MF, Balbi CB, Gómez KA, Pérez AR, Alloatti A. Immunization with lipopolysaccharide-activated dendritic cells generates a specific CD8+ T cell response that confers partial pro

tection against infection with Trypanosoma cruzi. Front Cell Infect Microbiol. 2022; 12:897133. doi: 10.3389/ fcimb.2022.897133.

Bromfield JJ, Sheldon IM. Lipopolysaccharide initiates inflam mation in bovine granulosa cells via the TLR4 pathway and perturbs oocyte meiotic progression in vitro. Endocrinology. 2011; 152(12):5029-40. doi: 10.1210/en.2011-1124.

Bromfield JJ, Sheldon IM. Lipopolysaccharide reduces the pri mordial follicle pool in the bovine ovarian cortex ex vivo and in the murine ovary in vivo. Biol Reprod. 2013;88(4):98- 1. doi:10.1095/biolreprod.112.106914.

Chanrot M, Guo Y, Dalin AM, Persson E, Båge R, Svensson A, Gustafsson H, Humblot P. Dose related effects of LPS on endometrial epithelial cell populations from dioestrus cows. Anim Reprod Sci. 2017; 177:12-24. doi: 10.1016/j.ani

reprosci.2016.12.002.

Cheong SH, Nydam DV, Galvão KN, Crosier BM, Gilbert RO. Cow-level and herd-level risk factors for subclini cal endometritis in lactating Holstein cows. J Dairy Sci. 2011;94(2):762-70. doi: 10.3168/jds.2010-3439.

Ciesielska A, Matyjek M, Kwiatkowska K. TLR4 and CD14 traf ficking and its influence on LPS-induced pro-inflamma tory signaling. Cell Mol Life Sci. 2021;78(4):1233-1261. doi: 10.1007/s00018-020-03656-y.

Davies D, Meade KG, Herath S, Eckersall PD, Gonzalez D, White JO, Conlan RS, O’Farrelly C, Sheldon IM. Toll-like recep tor and antimicrobial peptide expression in the bovine endometrium. Reprod Biol Endocrinol. 2008; 6:53. doi: 10.1186/1477-7827-6-53.

de Campos FT, Rincon JAA, Acosta DAV, Silveira PAS, Pradieé J, Corrêa MN, Gasperin BG, Pfeifer LFM, Barros CC, Pegoraro LMC, Schneider A. The acute effect of intrave nous lipopolysaccharide injection on serum and intrafol licular HDL components and gene expression in granulosa cells of the bovine dominant follicle. Theriogenology. 2017; 89:244-249. doi: 10.1016/j.theriogenology.2016.11.013.

Deb K, Chatturvedi MM, Jaiswal YK. Gram-negative bacterial endotoxin- induced infertility: a birds eye view. Gynecol Obstet Invest. 2004; 57(4):224-32. doi: 10.1159/000076761.

Dubey PK, Goyal S, Kathiravan P, Mishra BP, Gahlawat SK, Kataria RS. Sequence characterization of river buffalo Toll like receptor genes 1-10 reveals distinct relationship with cattle and sheep. Int J Immunogenet. 2013; 40(2):140-8. doi: 10.1111/j.1744-313X.2012.01135. x.

Eley A, Pacey AA, Galdiero M, Galdiero M, Galdiero F. Can Chlamydia trachomatis directly damage your sperm? Lancet Infect Dis. 2005;5(1):53-7. doi: 10.1016/S1473- 3099(04)01254-X.

Ferronato GA, Alvarado-Rincón JA, Maffi AS, Barbosa AA, Gasperin BG, Schneider A, Mondadori RG, Brauner CC,

Corrêa MN. Expression of genes associated with fertil ity in the uterus and oviduct of heifers challenged with lipopolysaccharide. Zygote. 2022; 12: 1-4.doi:10.1017/ S0967199421000745

Fitzgerald KA, Palsson-McDermott EM, Bowie AG, Jefferies CA, Mansell AS, Brady G, Brint E, Dunne A, Gray P, Harte MT, McMurray D, Smith DE, Sims JE, Bird TA, O’Neill LA. Mal (MyD88-adapter-like) is required for Toll-like receptor-4 signal transduction. Nature. 2001;413(6851):78-83. doi: 10.1038/35092578.

Forrest KK, Flores VV, Gurule SC, Soto-Navarro S, Shuster CB, Gifford CA, Gifford JAH. Effects of lipopolysaccha ride on follicular estrogen production and developmental competence in bovine oocytes. Anim Reprod Sci. 2022; 237:106927. doi: 10.1016/j.anireprosci.2022.106927.

Ghanem M, Shalaby AH, Sharawy S, Saleh N. Factors leading to endometritis in dairy cows in Egypt with special refer ence to reproductive performance. J Reprod dev. 2002; 48(4):371-5. doi: 10.1262/jrd.48.371.

Hankittichai P, Buacheen P, Pitchakarn P, Na Takuathung M, Wikan N, Smith DR, Potikanond S, Nimlamool W. Artocarpuslakoocha Extract Inhibits LPS-Induced Inflammatory Response in RAW 264.7 Macrophage Cells. Int J Mol Sci. 2020;21(4):1355. doi: 10.3390/

ijms21041355.

Heidari M, Kafi M, Mirzaei A, Asaadi A, Mokhtari A. Effects of follicular fluid of preovulatory follicles of repeat breeder dairy cows with subclinical endometritis on oocyte devel opmental competence. Anim Reprod Sci. 2019; 205:62-9. doi: 10.1016/j.anireprosci.2019.04.004.

Helmby H, Grencis RK. Essential role for TLR4 and MyD88 in the development of chronic intestinal nematode infec tion. Eur J Immunol. 2003;33(11):2974-9. doi: 10.1002/ eji.200324264.

Herath S, Fischer DP, Werling D, Williams EJ, Lilly ST, Dobson H, Bryant CE, Sheldon IM. Expression and function of Toll-like receptor 4 in the endometrial cells of the uterus. Endocrinology. 2006;147(1):562-70. doi: 10.1210/en.2005-

Herath S, Lilly ST, Santos NR, Gilbert RO, Goetze L, Bryant CE, White JO, Cronin J, Sheldon IM. Expression of genes asso ciated with immunity in the endometrium of cattle with disparate postpartum uterine disease and fertility. Reprod Biol Endocrinol. 2009; 7:55. doi: 10.1186/1477-7827-7-55.

Herath S, Williams EJ, Lilly ST, Gilbert RO, Dobson H, Bryant CE, Sheldon IM. Ovarian follicular cells have innate immune capabilities that modulate their endocrine func tion. Reproduction. 2007;134(5):683-93. doi: 10.1530/REP 07-0229.

Heydari S, Eidi A, Kouhkan F, Tvrda E, Mohammadi Sangcheshmeh A. Effects of increasing lipopolysaccharide concentrations on in vitro developmental competence of ovine oocytes. Anim Reprod. 2020;17(2): e20190125. doi: 10.1590/1984-3143-AR2019-0125.

Hoshino K, Takeuchi O, Kawai T, Sanjo H, Ogawa T, Takeda Y, Takeda K, Akira S. Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopoly saccharide: evidence for TLR4 as the Lps gene product. J Immunol. 1999; 162(7):3749-52.

Hvid M, Baczynska A, Deleuran B, Fedder J, Knudsen HJ, Christiansen G, Birkelund S. Interleukin-1 is the initiator of Fallopian tube destruction during Chlamydia tracho matis infection. Cell Microbiol. 2007; 9(12):2795-803. doi: 10.1111/j.1462-5822.2007.00996. x.

Ibrahim S, Salilew-Wondim D, Rings F, Hoelker M, Neuhoff C, Tholen E, Looft C, Schellander K, Tesfaye D. Expression pattern of inflammatory response genes and their regu latory micrornas in bovine oviductal cells in response to lipopolysaccharide: implication for early embryonic devel opment. PLoS One. 2015; 10(3): e0119388. doi: 10.1371/ journal.pone.0119388.

Janeway Jr CA, Medzhitov R. Innate immune recognition. Annu Rev Immunol. 2002; 20(1):197-216.

Kasimanickam R, Duffield TF, Foster RA, Gartley CJ, Leslie KE, Walton JS, Johnson WH. Endometrial cytology and ultra sonography for the detection of subclinical endometritis in postpartum dairy cows. Theriogenology. 2004; 62(1-2):9- 23. doi: 10.1016/j.theriogenology.2003.03.001.

Kim SJ, Kim HM. Dynamic lipopolysaccharide transfer cas cade to TLR4/MD2 complex via LBP and CD14. BMB Rep. 2017;50(2):55-57. doi: 10.5483/bmbrep.2017.50.2.011.

Kumar H, Kawai T, Akira S. Toll-like receptors and innate immu nity. Biochem Biophys Res Commun. 2009;388(4):621-5. doi: 10.1016/j.bbrc.2009.08.062.

LeBlanc SJ, Duffield TF, Leslie KE, Bateman KG, Keefe GP, Walton JS, Johnson WH. Defining and diagnosing postpar tum clinical endometritis and its impact on reproductive performance in dairy cows. J Dairy Sci. 2002;85(9):2223-36. doi: 10.3168/jds. S0022-0302(02)74302-6.

Magata F, Horiuchi M, Miyamoto A, Shimizu T. Lipopolysaccharide (LPS) inhibits steroid production in theca cells of bovine follicles in vitro: distinct effect of LPS on theca cell function in pre- and post-selection follicles. J Reprod Dev. 2014; 60: 280–287. doi:10.1262/jrd.2013-124.

Magata F, Shimizu T. Effect of lipopolysaccharide on develop mental competence of oocytes. Reprod Toxicol. 2017; 71:1- 7. doi: 10.1016/j.reprotox.2017.04.001.

Magata F. Lipopolysaccharide-induced mechanisms of ovarian dysfunction in cows with uterine inflammatory diseases. J Reprod Dev. 2020;66(4):311-317. doi: 10.1262/jrd.2020- 021.

Makvandi A, Kowsar R, Hajian M, Mahdavi AH, TanhaeiVash N, Nasr-Esfahani MH. Alpha lipoic acid reverses the nega tive effect of LPS on mouse spermatozoa and developmen tal competence of resultant embryos in vitro. Andrology. 2019;7(3):350-356. doi: 10.1111/andr.12596.

Matsushima N, Tanaka T, Enkhbayar P, Mikami T, Taga M, Yamada K, Kuroki Y. Comparative sequence analysis of leucine-rich repeats (LRRs) within vertebrate toll-like receptors. BMC Genomics. 2007; 8:124. doi: 10.1186/1471-

-8-124.

Medzhitov R. Toll-like receptors and innate immunity. Nat Rev Immunol. 2001; 1(2):135-45. doi: 10.1038/35100529. Mohammed ZA, Robinson RS, Harris R, McLaughlin Y, Turnbull KEM, Mann GE, WoadKJ.Detrimental effects of uterine disease and lipopolysaccharide on luteal angiogenesis. J Endocrinol. 2020; 245(1):79-92. doi: 10.1530/JOE-19-0443. Mokhtari S, Mahdavi AH, Hajian M, Kowsar R, Varnosfaderani SR, Nasr-Esfahani MH. The attenuation of the toxic effects of LPS on mouse pre-implantation development by alpha-lipoic acid. Theriogenology. 2020;143:139-147. doi: 10.1016/j.theriogenology.2019.12.008.

Moresco EM, LaVine D, Beutler B. Toll-like receptors. Current Biology. 2011;21(13): R488-93. doi: 10.1016/j. cub.2011.05.039.

O’Doherty AM, Di Fenza M, Kölle S. Lipopolysaccharide (LPS) disrupts particle transport, cilia function and sperm motil ity in an ex vivo oviduct model. Sci Rep. 2016; 6:24583. doi: 10.1038/srep24583.

Ota H, Igarashi S, Hatazawa J, Tanaka T. Endometriosis and free radicals. GynecolObstet Invest. 1999; 48 (Suppl 1): 29–35. doi:10.1159/000052866.

Parikh SS, Kavani FS, Parmar KH, Patbandha TK, Singh VK, Ahlawat AR, Kumar R. 2022. Diagnostic and therapeu tic management of subclinical endometritis in dairy bovine: A review. Anim Reprod Update. 2022; 2(2):1-11. Doi:10.48165/aru.2022.2.2.1.

Piersanti RL, Santos JEP, Sheldon IM, Bromfield JJ. Lipopolysaccharide and tumor necrosis factor-alpha alter gene expression of oocytes and cumulus cells during bovine in vitro maturation. MolReprod Dev. 2019; 86(12):1909-

doi: 10.1002/mrd.23288.

Rasekhi M, Mohammadi-Sangcheshmeh A, Daliri M, Bakhtiarizadeh M, Shariati V, Rahimi M, Hajarizadeh A, Nazari SA, Ross PJ, Tvrdá E. Transcriptional profile of

ovine oocytes matured under lipopolysaccharide treatment in vitro. Theriogenology. 2020; 157:70-78. doi: 10.1016/j. theriogenology.2020.07.034.

Rincon JAA, Gindri PC, Mion B, Giuliana de Ávila F, Barbosa AA, Maffi AS, Pradieé J, Mondadori RG, Corrêa MN, LigiaMargarethCantarelli P, Schneider A. Early embry onic development of bovine oocytes challenged with LPS in vitro or in vivo. Reproduction. 2019;158(5):453-463. doi: 10.1530/REP-19-0316.

Salleh N, Giribabu N. Leukemia inhibitory factor: roles in embryo implantation and in non-hormonal contra ception. Scientific World J. 2014; 2014: 201514. doi: 10.1155/2014/201514.

Sheldon IM, Cronin JG, Healey GD, Gabler C, Heuwieser W, Streyl D, Bromfield JJ, Miyamoto A, Fergani C & Dobson H Innate immunity and inflammation of the bovine female reproductive tract in health and disease. Reproduction. 2014; 148 R41–R51. doi:10.1530/REP-14-0163.

Sheldon IM, Price SB, Cronin J, Gilbert RO, Gadsby JE. Mechanisms of infertility associated with clinical and sub clinical endometritis in high producing dairy cattle. Reprod Domest Anim. 2009;44Suppl 3:1-9. doi: 10.1111/j.1439- 0531.2009.01465. x.

Shepel E, Grushka N, Makogon N, Sribna V, Pavlovych S, Yanchii R. Changes in DNA integrity and gene expression in ovarian follicular cells of lipopolysaccharide-treated female mice. Pharmacol Rep. 2018;70(6):1146-1149. doi: 10.1016/j.pharep.2018.06.005.

Shimizu T, Miyauchi K, Shirasuna K, Bollwein H, Magata F, Murayama C, Miyamoto A. Effects of lipopolysaccharide (LPS) and peptidoglycan (PGN) on estradiol production in bovine granulosa cells from small and large follicles. Toxicol In Vitro. 2012;26(7):1134-42. doi: 10.1016/j.tiv.2012.06.014.

Soto P, Natzke RP, Hansen PJ. Identification of possible media tors of embryonic mortality caused by mastitis: actions of lipopolysaccharide, prostaglandin F2alpha, and the nitric oxide generator, sodium nitroprussidedihydrate, on oocyte maturation and embryonic development in cattle. Am J Reprod Immunol. 2003;50(3):263-72. doi: 10.1034/j.1600- 0897.2003.00085. x.

Suzuki C, Yoshioka K, Iwamura S, Hirose H. Endotoxin induces delayed ovulation following endocrine aberration during the proestrous phase in Holstein heifers. Domest Anim Endocrinol. 2001;20(4):267-78. doi: 10.1016/s0739-

(01)00098-4.

Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell. 2010; 140(6):805-20. doi: 10.1016/j. cell.2010.01.022.

Turner EC, Hughes J, Wilson H, Clay M, Mylonas KJ, Kipari T, Duncan WC & Fraser HM Conditional ablation of macro phages disrupts ovarian vasculature. Reproduction. 2011; 141 821–831. doi:10.1530/REP-10-0327.

Walusimbi SS and Pate JL. Physiology and Endocrinology Symposium: role of immune cells in the corpus luteum. J Anim Sci. 2013; 91 1650–1659. doi:10.2527/jas.2012-6179.

Wiebe M, Pfarrer C, Górriz Martín L, Schmicke M, Hoedemaker M, Bollwein H, Heppelmann M. In vitro effects of lipopoly saccharides on bovine uterine contractility. Reprod Domest Anim. 2021;56(1):172-182. doi: 10.1111/rda.13862.

Wu R, Van der Hoek KH, Ryan NK, Norman RJ, Robker RL. Macrophage contributions to ovarian function. Human Reprod Update. 2004; 10 119–133. doi:10.1093/humupd/ dmh011.

Yilmaz O, Całka J, Bukowski R, Zalecki M, Wasowicz K, Jaroszewski JJ, Markiewicz W, Bulbul A, Ucar M. Nitric oxide in the bovine oviduct: influence on contractile activity and nitric oxide synthase isoforms localization. Theriogenology. 2012 77(7):1312-27. doi: 10.1016/j.ther

iogenology.2011.10.036.

Yu B, Hailman E, Wright SD. Lipopolysaccharide binding pro tein and soluble CD14 catalyze exchange of phospholipids. J Clin Invest. 1997;99(2):315-24. doi: 10.1172/JCI119160.

Zhao S, Pang Y, Zhao X, Du W, Hao H, Zhu H. Detrimental effects of lipopolysaccharides on maturation of bovine oocytes. Asian-Austra J Anim Sci. 2019; 32(8):1112-1121. doi: 10.5713/ajas.18.0540.

Zhao SJ, Pang YW, Zhao XM, Du WH, Hao HS, Zhu HB.Effects of lipopolysaccharide on maturation of bovine oocyte in vitro and its possible mechanisms. Oncotarget. 2017;8(3):4656. doi: 10.18632/oncotarget.13965.

Published

2023-03-07

How to Cite

Jinagal, S., Dutt, R., Thakur, S., Punetha, M., Sharma, M., Saini, S., … Kumar, D. (2023). Developmental Competence of Embryo vis-à-vis Lipopolysaccharide . Animal Reproduction Update , 3(1), 31–40. https://doi.org/10.48165/aru.2023.3.1.6