Hostname: page-component-76fb5796d-vfjqv Total loading time: 0 Render date: 2024-04-26T13:01:58.924Z Has data issue: false hasContentIssue false
  • English
  • Français

Proliferation-apoptosis balance in Staphylococcus aureus chronically infected bovine mammary glands during involution

Published online by Cambridge University Press:  13 March 2017

Carolina S Andreotti ,
Elizabet A L Pereyra ,
Sofía C Sacco ,
Celina Baravalle ,
María S Renna ,
Hugo H Ortega ,
Luis F Calvinho  and
Bibiana E Dallard
Carolina S Andreotti
Affiliation:
Laboratorio de Biología Celular y Molecular Aplicada, Instituto de Ciencias Veterinarias del Litoral (ICIVET-Litoral), Universidad Nacional del Litoral (UNL)/Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET), Esperanza, Santa Fe, Argentina
Elizabet A L Pereyra
Affiliation:
Laboratorio de Biología Celular y Molecular Aplicada, Instituto de Ciencias Veterinarias del Litoral (ICIVET-Litoral), Universidad Nacional del Litoral (UNL)/Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET), Esperanza, Santa Fe, Argentina Facultad de Ciencias Veterinarias, Universidad Nacional del Litoral (UNL), Esperanza, Santa Fe, Argentina
Sofía C Sacco
Affiliation:
Laboratorio de Biología Celular y Molecular Aplicada, Instituto de Ciencias Veterinarias del Litoral (ICIVET-Litoral), Universidad Nacional del Litoral (UNL)/Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET), Esperanza, Santa Fe, Argentina Facultad de Ciencias Veterinarias, Universidad Nacional del Litoral (UNL), Esperanza, Santa Fe, Argentina
Celina Baravalle
Affiliation:
Laboratorio de Biología Celular y Molecular Aplicada, Instituto de Ciencias Veterinarias del Litoral (ICIVET-Litoral), Universidad Nacional del Litoral (UNL)/Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET), Esperanza, Santa Fe, Argentina Facultad de Ciencias Veterinarias, Universidad Nacional del Litoral (UNL), Esperanza, Santa Fe, Argentina
María S Renna
Affiliation:
Laboratorio de Biología Celular y Molecular Aplicada, Instituto de Ciencias Veterinarias del Litoral (ICIVET-Litoral), Universidad Nacional del Litoral (UNL)/Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET), Esperanza, Santa Fe, Argentina
Hugo H Ortega
Affiliation:
Laboratorio de Biología Celular y Molecular Aplicada, Instituto de Ciencias Veterinarias del Litoral (ICIVET-Litoral), Universidad Nacional del Litoral (UNL)/Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET), Esperanza, Santa Fe, Argentina Facultad de Ciencias Veterinarias, Universidad Nacional del Litoral (UNL), Esperanza, Santa Fe, Argentina
Luis F Calvinho
Affiliation:
Facultad de Ciencias Veterinarias, Universidad Nacional del Litoral (UNL), Esperanza, Santa Fe, Argentina Estación Experimental Agropecuaria Rafaela, Instituto Nacional de Tecnología Agropecuaria (INTA), Rafaela, Santa Fe, Argentina
Bibiana E Dallard*
Affiliation:
Laboratorio de Biología Celular y Molecular Aplicada, Instituto de Ciencias Veterinarias del Litoral (ICIVET-Litoral), Universidad Nacional del Litoral (UNL)/Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET), Esperanza, Santa Fe, Argentina Facultad de Ciencias Veterinarias, Universidad Nacional del Litoral (UNL), Esperanza, Santa Fe, Argentina
*
*For correspondence; e-mail: bdallard@fcv.unl.edu.ar
Get access Rights & Permissions [Opens in a new window]

Abstract

The objective of this study was to determine whether Staphylococcus aureus chronic intramammary infection (IMI) influences expression of proteins related to regulation of proliferation and apoptosis processes and proliferation/apoptosis index during active involution in bovine mammary gland. Twenty-one Holstein non-pregnant cows in late lactation either uninfected or with chronic naturally acquired S. aureus IMI were included in this study. Cows were slaughtered at 7, 14 and 21 d after cessation of milking and samples for immunohistochemical analysis were taken. Protein expression of Bcl-2, Bax, Fas and active caspase-3 in mammary tissue was significantly affected by chronic S. aureus IMI, all showing increased immunoexpression in S. aureus-infected quarters at all involution stages. The percentage of apoptotic cells was increased by IMI in both mammary parenchyma and stroma, and the percentage of parenchymal and stromal cell proliferation was also increased. The proliferation/apoptosis ratio was significantly increased by IMI only in stromal cells. This imbalance to favour proliferation in S. aureus-infected mammary quarters could be one of the underlying causes that induce aberrant involution with permanence of nonsecretory tissue and increase of stromal components.

Keywords

MastitisStaphylococcus aureusapoptosisproliferationactive involution
Type
Research Article
Information
Journal of Dairy Research , Volume 84 , Issue 2 , May 2017 , pp. 181 - 189
Copyright
Copyright © Proprietors of Journal of Dairy Research 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Andreotti, CS, Pereyra, EA, Baravalle, C, Renna, MS, Ortega, HH, Calvinho, LF & Dallard, BE 2014 Staphylococcus aureus chronic intramammary infection modifies protein expression of transforming growth factor beta (TGF-β) subfamily components during active involution. Research in Veterinary Science 96 5–14 CrossRefGoogle ScholarPubMed
Bayles, KW, Wesson, CA, Liou, LE, Fox, LK, Bohach, GA & Trumble, WR 1998 Intracellular Staphylococcus aureus escapes the endosome and induces apoptosis in epithelial cells. Infection and Immunity 66 336–442 CrossRefGoogle ScholarPubMed
Capuco, AV, Akers, RM & Smith, JJ 1997 Mammary growth in Holstein cows during the dry period: quantification of nucleic acids and histology. Journal of Dairy Science 80 477–487 Google Scholar
Colitti, M 2012 Bcl-2 family of proteins and mammary cellular fate. Anatomia, Histologia, Embryologia 41 237–247 CrossRefGoogle ScholarPubMed
Dallard, BE, Ruffino, V, Heffel, S & Calvinho, LF 2007 Effect of a biological response modifier on expression of growth factors and cellular proliferation at drying off. Journal of Dairy Science 90 2229–2240 Google Scholar
Dallard, BE, Baravalle, C, Ortega, HH, Ruffino, V, Heffel, S & Calvinho, LF 2008 Effect of a biological response modifier on cellular death mechanisms at drying off. Journal of Dairy Research 75 167–175 Google Scholar
Dallard, BE, Ortega, HH, Iguzquiza, IA, Salvetti, NR, Quaino, OA & Calvinho, LF 2010 The effect of a single intramammary infusion of a biological response modifier in cows at drying off. Veterinary Research Communications 34 519–532 Google Scholar
Dallard, BE, Baravalle, C, Andreotti, C, Ortega, HH, Neder, V & Calvinho, LF 2011 Intramammary inoculation of Panax ginseng extract in cows at drying off enhances early mammary involution. Journal of Dairy Research 78 63–71 Google Scholar
Federation of Animal Science Societies (FASS) 2010 Guide for the Care and Use of Agricultural Animals in Teaching and Research. 3rd ed. Federation of Animal Science Societies, Champaign, IL Google Scholar
Halasa, T, Nielen, M, Huirne, RBM & Hogeveen, H 2009 Stochastic bio-economic model of bovine intramammary infection. Livestock Science 124 295–305 CrossRefGoogle Scholar
Hu, Q, Cui, X, Tao, L, Xiu, L, Wang, T & Wang, X 2014 Staphylococcus aureus induces apoptosis in primary bovine mammary epithelial cells through Fas-FADD death receptor-linked caspase-8 signaling. DNA and Cell Biology 33 388–397 Google Scholar
Kikuchi, H, Kuribayashi, F & Imajoh-Ohmi, S 2014 Down-regulation of Fas-mediated apoptosis by plasma transglutaminase factor XIII that catalyzes fetal-specific cross-link of the Fas molecule. Biochemical and Biophysical Research Communications 443 13–17 Google Scholar
Krzymińska, S, Szczuka, E & Kaznowski, A 2012 Staphylococcus haemolyticus strains target mitochondria and induce caspase-dependent apoptosis of macrophages. Antonie Van Leeuwenhoek 102 611–620 Google Scholar
Norgaard, JV, Theil, PK, Sorensen, MT & Sejrsen, K 2008 Cellular mechanisms in regulating mammary cell turnover during lactation and dry period in dairy cows. Journal of Dairy Science 91 2319–2327 CrossRefGoogle ScholarPubMed
Sladek, Z, Rysanek, D, Ryznarova, H & Faldyna, M 2005 Neutrophil apoptosis during experimentally induced Staphylococcus aureus mastitis. Veterinary Research 36 629–643 Google Scholar
Slama, P, Sladek, Z, Rysanek, D & Langrova, T 2009 Effect of Staphylococcus aureus and Streptococcus uberis on apoptosis of bovine mammary gland lymphocytes. Research in Veterinary Science 87 233–238 Google Scholar
Song, J, Sapi, E, Brown, W, Nilsen, J, Tartaro, K, Kacinski, BM, Craft, J, Naftolin, F & Mor, G 2000 Roles of Fas and Fas ligand during mammary gland remodeling. Journal of Clinical Investigation 106 1209–1220 Google Scholar
Sordillo, LM & Nickerson, SC 1988 Morphologic changes in the bovine mammary gland during involution and lactogenesis. American Journal of Veterinary Research 49 1112–1120 Google ScholarPubMed
Wang, JH, Zhou, YJ & He, P 2010 Staphylococcus aureus induces apoptosis of human monocytic U937 cells via NF-kappaB signaling pathways. Microbial Pathogenesis 49 252–259 Google Scholar
Wesson, CA, Deringer, J, Liou, LE, Bayles, KW, Bohach, GA & Trumble, WR 2000 Apoptosis induced by Staphylococcus aureus in epithelial cells utilizes a mechanism involving caspases 8 and 3. Infection and Immunity 68 2998–3001 Google Scholar
Yin, XM 2000 Signal transduction mediated by Bid, a pro-death Bcl-2 family proteins, connects the death receptor and mitochondria apoptosis pathways. Cell Research 10 161–167 Google Scholar
Zarzynska, J & Motyl, T 2008 Apoptosis and autophagy in involuting bovine mammary gland. Journal of Physiology and Pharmacology 59 275–288 Google Scholar
Zecconi, A & Scali, F 2013 Staphylococcus aureus virulence factors in evasion from innate immune defenses in human and animal diseases. Immunology Letters 150 12–22 CrossRefGoogle ScholarPubMed
Zhang, H, Heim, J & Meyhack, B 1998 Redistribution of Bax from cytosol to membranes is induced by apoptotic stimuli and is an early step in the apoptotic pathway. Biochemical and Biophysical Research Communication 251 454–459 Google Scholar
Zhao, X & Lacasse, P 2008 Mammary tissue damage during bovine mastitis: causes and control. Journal of Animal Science 86 57–65 Google Scholar