Local Heat Treatment of Goat Udders Influences Innate Immune Functions in Mammary Glands.
Antimicrobial components
Heat stress
Mammary gland
Ruminant
Journal
Journal of mammary gland biology and neoplasia
ISSN: 1573-7039
Titre abrégé: J Mammary Gland Biol Neoplasia
Pays: United States
ID NLM: 9601804
Informations de publication
Date de publication:
12 2021
12 2021
Historique:
received:
16
11
2021
accepted:
05
01
2022
pubmed:
12
1
2022
medline:
10
5
2022
entrez:
11
1
2022
Statut:
ppublish
Résumé
Heat stress and mastitis adversely affect milk production in dairy ruminants. Although the udder temperature is elevated in both conditions, the influence of this local temperature rise on milk production and immune function of ruminant mammary glands remains unclear. To address this question, we heated the mammary glands of goats by covering one half of the udder with a disposable heating pad for 24 h, the other uncovered half served as a control. Sixteen Tokara goats (1-5 parity) and three Shiba goats (1-2 parity) at the mid-lactation stage were individually housed, fed 0.6 kg of hay cubes and 0.2 kg of barley per day, and had free access to water and trace-mineralized salt blocks. Milk samples were collected every 6 h for 24 h after covering (n = 16), and deep mammary gland tissue areas were collected after 24 h (n = 5). The concentrations of antimicrobial components [lactoferrin, β-defensin-1, cathelicidin-2, cathelicidin-7, and immunoglobulin A (IgA)] in milk were measured by the enzyme-linked immunosorbent assay (ELISA). The localization of IgA was examined by immunohistochemistry. The mRNA expression and protein concentrations of C-C motif chemokine ligand-28 (CCL-28) and interleukin (IL)-8 in the mammary gland tissue were measured using quantitative polymerase chain reaction and ELISA, respectively. The somatic cell count in milk was significantly higher in the local heat-treatment group than in the control group after 12 h of treatment. The treatment group had significantly higher concentrations of cathelicidin-2 and IgA than the control group after 24 h of treatment. In addition, the number of IgA-positive cells in the mammary stromal region and the concentration of CCL-28 in the mammary glands were increased by local heat treatment. In conclusion, a local rise in udder temperature enhanced the innate immune function in mammary glands by increasing antimicrobial components.
Identifiants
pubmed: 35015201
doi: 10.1007/s10911-022-09509-7
pii: 10.1007/s10911-022-09509-7
doi:
Substances chimiques
Anti-Infective Agents
0
Immunoglobulin A
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
387-397Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
West JW. Effects of heat-stress on production in dairy cattle. J Dairy Sci. 2003;86:2131–44. https://doi.org/10.3168/jds.S0022-0302(03)73803-X .
doi: 10.3168/jds.S0022-0302(03)73803-X
pubmed: 12836950
Bobbo T, Ruegg PL, Stocco G, Fiore E, Gianesella M, Morgante M, et al. Associations between pathogen-specific cases of subclinical mastitis and milk yield, quality, protein composition, and cheese-making traits in dairy cows. J Dairy Sci. 2017;100:4868–83. https://doi.org/10.3168/jds.2016-12353 .
doi: 10.3168/jds.2016-12353
pubmed: 28365113
Berman A, Folman Y, Kaim M, Mamen M, Herz Z, Wolfenson D, et al. Upper critical temperatures and forced ventilation effects for high-yielding dairy cows in a subtropical climate. J Dairy Sci. 1985;68:1488–95. https://doi.org/10.3168/jds.S0022-0302(85)80987-5 .
doi: 10.3168/jds.S0022-0302(85)80987-5
pubmed: 4019887
Yano M, Shimadzu H, Endo T. Modelling temperature effects on milk production: A study on Holstein cows at a Japanese farm. Springerplus. 2014;3:129. https://doi.org/10.1186/2193-1801-3-129 .
doi: 10.1186/2193-1801-3-129
pubmed: 24741472
pmcid: 3979979
Sathiyabarathi M, Jeyakumar S, Manimaran A, Pushpadass HA, Sivaram M, Ramesha KP, et al. Investigation of body and udder skin surface temperature differentials as an early indicator of mastitis in Holstein Friesian crossbred cows using digital infrared thermography technique. Vet World. 2016;9:1386–91. https://doi.org/10.14202/vetworld.2016.1386-1391
Hovinen M, Siivonen J, Taponen S, Hänninen L, Pastell M, Aisla AM, et al. Detection of clinical mastitis with the help of a thermal camera. J Dairy Sci. 2008;91:4592–8. https://doi.org/10.3168/jds.2008-1218 .
doi: 10.3168/jds.2008-1218
pubmed: 19038934
Borellini F, Oka T. Growth control and differentiation in mammary epithelial cells. Environ Health Perspect. 1989;80:85–99. https://doi.org/10.1289/ehp.898085 .
doi: 10.1289/ehp.898085
pubmed: 2647487
pmcid: 1567615
Huang YQ, Morimoto K, Hosoda K, Yoshimura Y, Isobe N. Differential immunolocalization between lingual antimicrobial peptide and lactoferrin in mammary gland of dairy cows. Vet Immunol Immunopathol. 2012;145:499–504. https://doi.org/10.1016/j.vetimm.2011.10.017 .
doi: 10.1016/j.vetimm.2011.10.017
pubmed: 22112298
Zarzosa-Moreno D, Avalos-Gómez C, Ramírez-Texcalco LS, Torres-López E, Ramírez-Mondragón R, Hernández-Ramírez JO, et al. Lactoferrin and its derived peptides: An alternative for combating virulence mechanisms developed by pathogens. Molecules. 2020;25. https://doi.org/10.3390/molecules25245763
Chanu KV, Thakuria D, Kumar S. Antimicrobial peptides of buffalo and their role in host defenses. Vet World. 2018;11:192–200. https://doi.org/10.14202/vetworld.2018.192-200
Wheeler TT, Smolenski GA, Harris DP, Gupta SK, Haigh BJ, Broadhurst MK, et al. hosts. Host-Defence-related proteins in cows’ milk Animal. 2012;6:415–22. https://doi.org/10.1017/S1751731111002151 .
doi: 10.1017/S1751731111002151
pubmed: 22436220
Ganz T. Defensins: Antimicrobial peptides of innate immunity. Nat Rev Immunol. 2003;3:710–20. https://doi.org/10.1038/nri1180 .
doi: 10.1038/nri1180
pubmed: 12949495
Yeung AT, Gellatly SL, Hancock RE. Multifunctional cationic host defence peptides and their clinical applications. Cell Mol Life Sci. 2011;68:2161–76. https://doi.org/10.1007/s00018-011-0710-x .
doi: 10.1007/s00018-011-0710-x
pubmed: 21573784
Zhang GW, Lai SJ, Yoshimura Y, Isobe N. Expression of cathelicidins mRNA in the goat mammary gland and effect of the intramammary infusion of lipopolysaccharide on milk cathelicidin-2 concentration. Vet Microbiol. 2014;170:125–34. https://doi.org/10.1016/j.vetmic.2014.01.029 .
doi: 10.1016/j.vetmic.2014.01.029
pubmed: 24572177
Loor JJ, Moyes KM, Bionaz M. Functional adaptations of the transcriptome to mastitis-causing pathogens: The mammary gland and beyond. J Mammary Gland Biol Neoplasia. 2011;16:305–22. https://doi.org/10.1007/s10911-011-9232-2 .
doi: 10.1007/s10911-011-9232-2
pubmed: 21968536
Brandtzaeg P. Secretory IgA: Designed for anti-microbial defense. Front Immunol. 2013;4:222. https://doi.org/10.3389/fimmu.2013.00222 .
doi: 10.3389/fimmu.2013.00222
pubmed: 23964273
pmcid: 3734371
Niimi K, Usami K, Fujita Y, Abe M, Furukawa M, Suyama Y, et al. Development of immune and microbial environments is independently regulated in the mammary gland. Mucosal Immunol. 2018;11:643–53. https://doi.org/10.1038/mi.2017.90 .
doi: 10.1038/mi.2017.90
pubmed: 29346344
Wilson E, Butcher EC. CCL28 controls immunoglobulin (Ig)A plasma cell accumulation in the lactating mammary gland and IgA antibody transfer to the neonate. J Exp Med. 2004;200:805–9. https://doi.org/10.1084/jem.20041069 .
doi: 10.1084/jem.20041069
pubmed: 15381732
pmcid: 2211970
Kobayashi K, Tsugami Y, Matsunaga K, Suzuki T, Nishimura T. Moderate high temperature condition induces the lactation capacity of mammary epithelial cells through control of STAT3 and STAT5 signaling. J Mammary Gland Biol Neoplasia. 2018;23:75–88. https://doi.org/10.1007/s10911-018-9393-3 .
doi: 10.1007/s10911-018-9393-3
pubmed: 29633073
Morad H, Luqman S, Tan CH, Swann V, McNaughton PA. TRPM2 ion channels steer neutrophils towards a source of hydrogen peroxide [Sci. Rep.:2021:11, 9339]
Zierler S, Hampe S, Nadolni W. TRPM channels as potential therapeutic targets against pro-inflammatory diseases. Cell Calcium. 2017;67:105–15. https://doi.org/10.1016/j.ceca.2017.05.002 .
doi: 10.1016/j.ceca.2017.05.002
pubmed: 28549569
Inada H, Iida T, Tominaga M. Different expression patterns of TRP genes in murine B and T lymphocytes. Biochem Biophys Res Commun. 2006;350:762–7. https://doi.org/10.1016/j.bbrc.2006.09.111 .
doi: 10.1016/j.bbrc.2006.09.111
pubmed: 17027915
Natale VA, McCullough KC. Macrophage culture: Influence of species-specific incubation temperature. J Immunol Methods. 1998;214:165–74. https://doi.org/10.1016/s0022-1759(98)00055-6 .
doi: 10.1016/s0022-1759(98)00055-6
pubmed: 9692868
Palackdharry S, Sadd BM, Vogel LA, Bowden RM. The effect of environmental temperature on reptilian peripheral blood B cell functions. Horm Behav. 2017;88:87–94. https://doi.org/10.1016/j.yhbeh.2016.10.008 .
doi: 10.1016/j.yhbeh.2016.10.008
pubmed: 27816625
Günther J, Petzl W, Zerbe H, Schuberth HJ, Koczan D, Goetze L, et al. Lipopolysaccharide priming enhances expression of effectors of immune defence while decreasing expression of pro-inflammatory cytokines in mammary epithelia cells from cows. BMC Genomics. 2012;13:17. https://doi.org/10.1186/1471-2164-13-17 .
doi: 10.1186/1471-2164-13-17
pubmed: 22235868
pmcid: 3315725
Suzuki N, Yuliza Purba F, Hayashi Y, Nii T, Yoshimura Y, Isobe N. Seasonal variations in the concentration of antimicrobial components in milk of dairy cows. Anim Sci J. 2020;91: e13427. https://doi.org/10.1111/asj.13427 .
doi: 10.1111/asj.13427
pubmed: 32696553
Bernabucci U, Lacetera N, Baumgard LH, Rhoads RP, Ronchi B, Nardone A. Metabolic and hormonal acclimation to heat stress in domesticated ruminants. Animal. 2010;4:1167–83. https://doi.org/10.1017/S175173111000090X .
doi: 10.1017/S175173111000090X
pubmed: 22444615
Isobe N, Matsukawa S, Kubo K, Ueno K, Sugino T, Nii T, Yoshimura Y. Effects of oral administration of colostrum whey in peripartum goat on antimicrobial peptides in postpartum milk. Anim Sci J. 2020;91:e13365. https://doi.org/10.1111/asj.13365 .
Purba FY, Ueda J, Nii T, Yoshimura Y, Isobe N. Effects of intrauterine infusion of bacterial lipopolysaccharides on the mammary gland inflammatory response in goats. Vet Immunol Immunopathol. 2020;219: 109972. https://doi.org/10.1016/j.vetimm.2019.109972 .
doi: 10.1016/j.vetimm.2019.109972
pubmed: 31733501
Kuwahara K, Yoshimura Y, Isobe N. Effect of steroid hormones on the innate immune response induced by Staphylococcus aureus in the goat mammary gland. Reprod Domest Anim. 2017;52:579–84. https://doi.org/10.1111/rda.12948 .
doi: 10.1111/rda.12948
pubmed: 28295702
Matsukawa S, Ueno K, Sugino T, Yoshimura Y, Isobe N. Effects of colostrum whey on immune function in the digestive tract of goats. Anim Sci J. 2018;89:1152–60. https://doi.org/10.1111/asj.13027 .
doi: 10.1111/asj.13027
pubmed: 29766609
Srisaikham S, Suksombat W, Yoshimura Y, Isobe N. Goat cathelicidin-2 is secreted by blood leukocytes regardless of lipopolysaccharide stimulation. Anim Sci J. 2016;87:423–7. https://doi.org/10.1111/asj.12438 .
doi: 10.1111/asj.12438
pubmed: 26212721
Isobe N, Nakamura J, Nakano H, Yoshimura Y. Existence of functional lingual antimicrobial peptide in bovine milk. J Dairy Sci. 2009;92:2691–5. https://doi.org/10.3168/jds.2008-1940 .
doi: 10.3168/jds.2008-1940
pubmed: 19448002
Zhang GW, Lai SJ, Yoshimura Y, Isobe N. Messenger RNA expression and immunolocalization of psoriasin in the goat mammary gland and its milk concentration after an intramammary infusion of lipopolysaccharide. Vet J. 2014;202:89–93. https://doi.org/10.1016/j.tvjl.2014.06.013 .
doi: 10.1016/j.tvjl.2014.06.013
pubmed: 25023088
Hunziker W, Kraehenbuhl JP. Epithelial transcytosis of immunoglobulins. J Mammary Gland Biol Neoplasia. 1998;3:287–302. https://doi.org/10.1023/a:1018715511178 .
doi: 10.1023/a:1018715511178
pubmed: 10819515
Brandtzaeg P. The mucosal immune system and its integration with the mammary glands. J Pediatr. 2010;156(Suppl):S8-15. https://doi.org/10.1016/j.jpeds.2009.11.014 .
doi: 10.1016/j.jpeds.2009.11.014
pubmed: 20105666
Bowman EP, Kuklin NA, Youngman KR, Lazarus NH, Kunkel EJ, Pan J, et al. The intestinal chemokine thymus-expressed chemokine (CCL25) attracts IgA antibody-secreting cells. J Exp Med. 2002;195:269–75. https://doi.org/10.1084/jem.20010670 .
doi: 10.1084/jem.20010670
pubmed: 11805153
pmcid: 2193602
Wang W, Soto H, Oldham ER, Buchanan ME, Homey B, Catron D, et al. Identification of a novel chemokine (CCL28), which binds CCR10 (GPR2). J Biol Chem. 2000;275:22313–23. https://doi.org/10.1074/jbc.M001461200 .
doi: 10.1074/jbc.M001461200
pubmed: 10781587
Distelhorst K, Voyich J, Wilson E. Partial characterization and distribution of the chemokines CCL25 and CCL28 in the bovine system. Vet Immunol Immunopathol. 2010;138:134–8. https://doi.org/10.1016/j.vetimm.2010.07.008 .
doi: 10.1016/j.vetimm.2010.07.008
pubmed: 20688401
Mohan T, Deng L, Wang BZ. CCL28 chemokine: An anchoring point bridging innate and adaptive immunity. Int Immunopharmacol. 2017;51:165–70. https://doi.org/10.1016/j.intimp.2017.08.012 .
doi: 10.1016/j.intimp.2017.08.012
pubmed: 28843907
pmcid: 5755716
Ezzat Alnakip M, Quintela-Baluja M, Böhme K, Fernández-No I, Caamaño-Antelo S, Calo-Mata P, et al. The immunology of mammary gland of dairy ruminants between healthy and inflammatory conditions. J Vet Med. 2014;2014: 659801. https://doi.org/10.1155/2014/659801 .
doi: 10.1155/2014/659801
pubmed: 26464939
pmcid: 4590879
Purba FY, Ishimoto Y, Nii T, Yoshimura Y, Isobe N. Effect of temporary cessation of milking on the innate immune components in goat milk. J Dairy Sci. 2021;104:10374–81. https://doi.org/10.3168/jds.2021-20564 .
doi: 10.3168/jds.2021-20564
pubmed: 34218919
Isobe N, Morimoto K, Nakamura J, Yamasaki A, Yoshimura Y. Intramammary challenge of lipopolysaccharide stimulates secretion of lingual antimicrobial peptide into milk of dairy cows. J Dairy Sci. 2009;92:6046–51. https://doi.org/10.3168/jds.2009-2594 .
doi: 10.3168/jds.2009-2594
pubmed: 19923607
Purba FY, Nii T, Yoshimura Y, Isobe N. Short communication: Production of antimicrobial peptide S100A8 in the goat mammary gland and effect of intramammary infusion of lipopolysaccharide on S100A8 concentration in milk. J Dairy Sci. 2019;102:4674–81. https://doi.org/10.3168/jds.2018-15396 .
doi: 10.3168/jds.2018-15396
pubmed: 30852007
Akers RM, Nickerson SC. Mastitis and its impact on structure and function in the ruminant mammary gland. J Mammary Gland Biol Neoplasia. 2011;16:275–89. https://doi.org/10.1007/s10911-011-9231-3 .
doi: 10.1007/s10911-011-9231-3
pubmed: 21968535
Kiku Y, Ozawa T, Takahashi H, Kushibiki S, Inumaru S, Shingu H, et al. Effect of intramammary infusion of recombinant bovine GM-CSF and IL-8 on CMT score, somatic cell count, and milk mononuclear cell populations in Holstein cows with Staphylococcus aureus subclinical mastitis. Vet Res Commun. 2017;41:175–82. https://doi.org/10.1007/s11259-017-9684-y .
doi: 10.1007/s11259-017-9684-y
pubmed: 28281038
Watanabe A, Yagi Y, Shiono H, Yokomizo Y. Effect of intramammary infusion of tumour necrosis factor-alpha on milk protein composition and induction of acute-phase protein in the lactating cow. J Vet Med B Infect Dis Vet Public Health. 2000;47:653–62. https://doi.org/10.1046/j.1439-0450.2000.00400.x .
doi: 10.1046/j.1439-0450.2000.00400.x
pubmed: 11244866
Wellnitz O, Arnold ET, Bruckmaier RM. Lipopolysaccharide and lipoteichoic acid induce different immune responses in the bovine mammary gland. J Dairy Sci. 2011;94:5405–12. https://doi.org/10.3168/jds.2010-3931 .
doi: 10.3168/jds.2010-3931
pubmed: 22032363
Bruckmaier RM, Weiss D, Wiedemann M, Schmitz S, Wendl G. Changes of physicochemical indicators during mastitis and the effects of milk ejection on their sensitivity. J Dairy Res. 2004;71:316–21. https://doi.org/10.1017/s0022029904000366 .
doi: 10.1017/s0022029904000366
pubmed: 15354578