Impact of an acute heat shock during in vitro maturation on interleukin 6 and its associated receptor component transcripts in bovine cumulus-oocyte complexes
Julia R. Rowinski; Louisa A. Rispoli; Rebecca R. Payton; Liesel G. Schneider; F. Neal Schrick; Kyle J. McLean; J. Lannett Edwards
Armstrong DV. Heat stress interaction with shade and cooling. J Dairy Sci. 1994;77(7):2044-50.
Assidi M, Dieleman SJ, Sirard MA. Cumulus cell gene expression following the LH surge in bovine preovulatory follicles: potential early markers of oocyte competence. Reproduction. 2010;140(6):835-52.
Botigelli RC, Razza EM, Pioltine EM, Fontes PK, Schwarz KRL, Leal CLV, Nogueira MFG. Supplementing
Campen KA, Abbott CR, Rispoli LA, Payton RR, Saxton AM, Edwards JL. Heat stress impairs gap junction communication and cumulus function of bovine oocytes. J Reprod Dev. 2018;64(5):385-92.
Canellada A, Alvarez I, Berod L, Gentile T. Estrogen and progesterone regulate the IL-6 signal transduction pathway in antibody secreting cells. J Steroid Biochem Mol Biol. 2008;111(3-5):255-61.
Castro EPLA, Hansen PJ. Interactions between oxygen tension and glucose concentration that modulate actions of heat shock on bovine oocytes during
Clark A, Matos DG, Jackson JA, Palmer SS, Tran CAT. Use of IL-6 type cytokines for maturation of oocytes. United States Patent. Appl. No. 10/998,080:Patent No. 8,071,375 B072. 2011.
Dang‐Nguyen TQ, Haraguchi S, Kikuchi K, Somfai T, Bodó S, Nagai T. Leukemia inhibitory factor promotes porcine oocyte maturation and is accompanied by activation of signal transducer and activator of transcription 3. Mol Reprod Dev. 2014;81(3):230-9.
del Collado M, Silveira JC, Sangalli JR, Andrade GM, Sousa LRDS, Silva LA, Meirelles FV, Perecin F. Fatty acid binding protein 3 and transzonal projections are involved in lipid accumulation during
Dunlap S, Vincent C. Influence of postbreeding thermal stress on conception rate in beef cattle. J Anim Sci. 1971;32(6):1216-8.
Ealy AD, Drost M, Hansen PJ. Developmental changes in embryonic resistance to adverse effects of maternal heat stress in cows. J Dairy Sci. 1993;76(10):2899-905.
Edwards JL, Bogart AN, Rispoli LA, Saxton AM, Schrick FN. Developmental competence of bovine embryos from heat-stressed ova. J Dairy Sci. 2009;92(2):563-70.
Edwards JL, Hansen PJ. Elevated temperature increases heat shock protein 70 synthesis in bovine two-cell embryos and compromises function of maturing oocytes. Biol Reprod. 1996;55(2):340-6.
Edwards JL, Saxton AM, Lawrence JL, Payton RR, Dunlap JR. Exposure to a physiologically relevant elevated temperature hastens
Elvinger F, Hansen P, Natzke R. Modulation of function of bovine polymorphonuclear leukocytes and lymphocytes by high temperature
Fallon G. Body temperature and fertilization in the cow. J Reprod Fertil. 1962;3(1):116-23.
Faundez R, Kawecka O, Aniołek O, Petrajtis-Gołobów M, Karska D, Gajewski Z. The influence of GM-CSF, IL-6 and TGF-α on
Faundez R, Kawecka O, Karska D, Petrajtis M, Gajewski Z. The influence of GM-CSF, IL-6 and TGF-α on the
Fisher AD, Morton R, Dempsey JM, Henshall JM, Hill JR. Evaluation of a new approach for the estimation of the time of the LH surge in dairy cows using vaginal temperature and electrodeless conductivity measurements. Theriogenology. 2008;70(7):1065-74.
Gaalaas R. Effect of atmospheric temperature on body temperature and respiration rate of Jersey cattle. J Dairy Sci. 1945;28(7):555-63.
Gearing D, Thut C, VandeBos T, Gimpel S, Delaney P, King J, Price V, Cosman D, Beckmann M. Leukemia inhibitory factor receptor is structurally related to the IL‐6 signal transducer, gp130. EMBO J. 1991;10(10):2839-48.
Heinrich PC, Behrmann I, Haan S, Hermanns HM, Muller-Newen G, Schaper F. Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem J. 2003;374(Pt 1):1-20.
Hibi M, Murakami M, Saito M, Hirano T, Taga T, Kishimoto T. Molecular cloning and expression of an IL-6 signal transducer, gp130. Cell. 1990;63(6):1149-57.
Higaki S, Miura R, Suda T, Andersson LM, Okada H, Zhang Y, Itoh T, Miwakeichi F, Yoshioka K. Estrous detection by continuous measurements of vaginal temperature and conductivity with supervised machine learning in cattle. Theriogenology. 2019;123:90-9.
Hooper LM, Payton RR, Rispoli LA, Saxton AM, Edwards JL. Impact of heat stress on germinal vesicle breakdown and lipolytic changes during
Hyttel P, Xu K, Smith S, Greve T. Ultrastructure of
Kyle BL, Kennedy AD, Small JA. Measurement of vaginal temperature by radiotelemetry for the prediction of estrus in beef cows. Theriogenology. 1998;49(8):1437-49.
Lawrence JL, Payton RR, Godkin JD, Saxton AM, Schrick FN, Edwards JL. Retinol improves development of bovine oocytes compromised by heat stress during maturation. J Dairy Sci. 2004;87(8):2449-54.
Lewis GS, Newman SK. Changes throughout estrous cycles of variables that might indicate estrus in dairy cows. J Dairy Sci. 1984;67(1):146-52.
Liu Z, Matos DG, Fan H-Y, Shimada M, Palmer S, Richards JS. Interleukin-6: an autocrine regulator of the mouse cumulus cell-oocyte complex expansion process. Endocrinology. 2009;150(7):3360-8.
Macabelli CH, Ferreira RM, Gimenes LU, de Carvalho NAT, Soares JG, Ayres H, Ferraz ML, Watanabe YF, Watanabe OY, Sangalli JR, Smith LC, Baruselli PS, Meirelles FV, Chiaratti MR. Reference gene selection for gene expression analysis of oocytes collected from dairy cattle and buffaloes during winter and summer. PLoS One. 2014;9(3):e93287.
Machelon V, Emilie D, Lefevre A, Nome F, Durand-Gasselin I, Testart J. Interleukin-6 biosynthesis in human preovulatory follicles: some of its potential roles at ovulation. J Clin Endocrinol Metab. 1994;79(2):633-42. PMid:7519193.
Mackiewicz A, Schooltink H, Heinrich PC, Rose-John S. Complex of soluble human IL-6-receptor/IL-6 up-regulates expression of acute-phase proteins. J Immunol. 1992;149(6):2021-7. PMid:1381393.
Miura R, Yoshioka K, Miyamoto T, Nogami H, Okada H, Itoh T. Estrous detection by monitoring ventral tail base surface temperature using a wearable wireless sensor in cattle. Anim Reprod Sci. 2017;180:50-7.
Mo X, Wu G, Yuan D, Jia B, Liu C, Zhu S, Hou Y. Leukemia inhibitory factor enhances bovine oocyte maturation and early embryo development. Mol Reprod Dev. 2014;81(7):608-18.
Mosher M, Ottobre J, Haibel G, Zartman D. Estrual rise in body temperature in the bovine II. The temporal relationship with ovulation. Anim Reprod Sci. 1990;23(2):99-107.
Nicola NA, Babon JJ. Leukemia inhibitory factor (LIF). Cytokine Growth Factor Rev. 2015;26(5):533-44.
Pavani KC, Rocha A, Baron E, Lourenço J, Faheem M, Silva FM. The effect of kinetic heat shock on bovine oocyte maturation and subsequent gene expression of targeted genes. Zygote. 2017;25(3):383-9.
Piccione G, Caola G, Refinetti R. Daily and estrous rhythmicity of body temperature in domestic cattle. BMC Physiol. 2003;3(1):7.
Rajamahendran R, Robinson J, Desbottes S, Walton JS. Temporal relationships among estrus, body temperature, milk yield, progesterone and luteinizing hormone levels, and ovulation in dairy cows. Theriogenology. 1989;31(6):1173-82.
Randi F, McDonald M, Duffy P, Kelly AK, Lonergan P. The relationship between external auditory canal temperature and onset of estrus and ovulation in beef heifers. Theriogenology. 2018;110:175-81.
Regassa A, Rings F, Hoelker M, Cinar U, Tholen E, Looft C, Schellander K, Tesfaye D. Transcriptome dynamics and molecular cross-talk between bovine oocyte and its companion cumulus cells. BMC Genomics. 2011;12(1):57.
Rispoli LA, Edwards JL, Pohler KG, Russell S, Somiari RI, Payton RR, Schrick FN. Heat-induced hyperthermia impacts the follicular fluid proteome of the periovulatory follicle in lactating dairy cows. PLoS One. 2019;14(12):e0227095.
Rispoli LA, Lawrence JL, Payton RR, Saxton AM, Schrock GE, Schrick FN, Middlebrooks BW, Dunlap JR, Parrish JJ, Edwards JL. Disparate consequences of heat stress exposure during meiotic maturation: embryo development after chemical activation vs fertilization of bovine oocytes. Reproduction. 2011;142(6):831-43.
Rispoli LA, Payton RR, Gondro C, Saxton AM, Nagle KA, Jenkins BW, Schrick FN, Edwards JL. Heat stress effects on the cumulus cells surrounding the bovine oocyte during maturation: altered matrix metallopeptidase 9 and progesterone production. Reproduction. 2013;146(2):193-207.
Roman-Ponce H, Thatcher W, Buffington D, Wilcox C, Van Horn H. Physiological and production responses of dairy cattle to a shade structure in a subtropical environment. J Dairy Sci. 1977;60(3):424-30.
Roth Z, Hansen PJ. Involvement of apoptosis in disruption of developmental competence of bovine oocytes by heat shock during maturation. Biol Reprod. 2004a;71(6):1898-906.
Roth Z, Hansen PJ. Sphingosine 1-phosphate protects bovine oocytes from heat shock during maturation. Biol Reprod. 2004b;71(6):2072-8.
Schrock GE, Saxton AM, Schrick FN, Edwards JL. Early
Seath D, Miller G. The relative importance of high temperature and high humidity as factors influencing respiration rate, body temperature, and pulse rate of dairy cows. J Dairy Sci. 1946;29(7):465-72.
Soto P, Smith LC. BH4 peptide derived from Bcl-xL and Bax-inhibitor peptide suppresses apoptotic mitochondrial changes in heat stressed bovine oocytes. Mol Reprod Dev. 2009;76(7):637-46.
Sugiyama S, McGowan M, Phillips N, Kafi M, Young M. Effects of increased ambient temperature during IVM and/or IVF on the
Suthar VS, Burfeind O, Patel JS, Dhami AJ, Heuwieser W. Body temperature around induced estrus in dairy cows. J Dairy Sci. 2011;94(5):2368-73.
Temme A, Traub O, Willecke K. Downregulation of connexin32 protein and gap-junctional intercellular communication by cytokine-mediated acute-phase response in immortalized mouse hepatocytes. Cell Tissue Res. 1998;294(2):345-50.
Tscherner A, Brown AC, Stalker L, Kao J, Dufort I, Sirard M-A, LaMarre J. STAT3 signaling stimulates miR-21 expression in bovine cumulus cells during
Turner H. Genetic variation of rectal temperature in cows and its relationship to fertility. Anim Sci. 1982;35(3):401-12.
Ulberg LC, Burfening PJ. Embryo death resulting from adverse environment on spermatozoa or ova. J Anim Sci. 1967;26(3):571-7.
Wang J, Liu Z, Sun Q, Xia S, Cui J, Yang L, An L, Zhang J, Su L, Su Y, Du F. Combined treatment with cysteamine and leukemia inhibitory factor promotes guinea pig oocyte meiosis
Wang Y, Liang N, Yao G, Tian H, Zhai Y, Yin Y, Sun F. Knockdown of TrkA in cumulus oocyte complexes (COCs) inhibits EGF-induced cumulus expansion by down-regulation of IL-6. Mol Cell Endocrinol. 2014;382(2):804-13.
Wolf J, Rose-John S, Garbers C. Interleukin-6 and its receptors: a highly regulated and dynamic system. Cytokine. 2014;70(1):11-20.
Wolfenson D, Roth Z. Impact of heat stress on cow reproduction and fertility. Anim Front. 2019;9(1):32-8.
Wooldridge LK, Ealy AD. Interleukin-6 increases inner cell mass numbers in bovine embryos. BMC Dev Biol. 2019;19(1):2.
Zakari A, Molokwu E, Osori D. Effects of rectal and ambient temperatures and humidity on conception rates. Theriogenology. 1981;16(3):331-6.
Zhandi M, Towhidi A, Nasr-Esfahani MH, Eftekhari-Yazdi P, Zare-Shahneh A. Unexpected detrimental effect of insulin like growth factor-1 on bovine oocyte developmental competence under heat stress. J Assist Reprod Genet. 2009;26(11-12):605-11.
Zhao X, Cang M, Gao X-y, Yang M, Yuan J, Zhu B, Wang Z, Liu D. Expression of interleukin–6 and interleukin-6 receptor in ovine oocytes during
Zolti M, Ben-Rafael Z, Meirom R, Shemesh M, Bider D, Mashiach S, Apte RN. Cytokine involvement in oocytes and early embryos. Fertil Steril. 1991;56(2):265-72.