Distinct behavior of bovine-associated staphylococci species in their ability to resist phagocytosis and trigger respiratory burst activity by blood and milk polymorphonuclear leukocytes in dairy cow

Author(s):Show less -

Souza, Rodrigo M. ^[1] ; Souza, Fernando N. ^{[2, 1, 3]} ; Batista, Camila F. ^[1] ; Piepers, Sofie ^[3] ; De Visscher, Anneleen ^[3] ; Santos, Kamila R. ^[1] ; Molinari, Paula C. ^{[4, 1]} ; Ferronatto, Jose A. ^[1] ; da Cunha, Adriano Franca ^[5] ; Blagitz, Maiara G. ^{[1, 6, 7]} ; da Silva, Guilherme G. ^[8] ; Renno, Francisco P. ^[8] ; Cerqueira, Monica M. O. P. ^[5] ; Heinemann, Marcos B. ^[9] ; De Vliegher, Sarne ^[3] ; Della Libera, Alice M. M. P. ^[1]

Affiliation

^[1] Univ Sao Paulo, Fac Med Vet & Zootecnia, Dept Clin Med, Vet Clin Immunol Res Grp, Av Prof Dr Orlando Marques de Paiva 87, BR-05508270 Sao Paulo - Brazil

^[2] Univ Fed Paraiba, Programa Posgrad Ciencia Anim, BR-58397000 Areia - Brazil

^[3] Univ Ghent, Fac Vet Med, M Team & Mastitis & Milk Qual Res Unit, Dept Reprod Obstet & Herd Hlth, Salisburylaan 133, B-9820 Merelbeke - Belgium

^[4] Univ Florida, Dept Anim Sci, Gainesville, FL 32611 - USA

^[5] Univ Fed Minas Gerais, Dept Tecnol & Inspecao Prod Origem Anim, Escola Vet, BR-31270010 Belo Horizonte, MG - Brazil

^[6] Univ Fed Fronteira Sul, Curso Med Vet, Campus Realeza, BR-85770000 Realeza - Brazil

^[7] Programa Posgrad Saude Bem Estar & Prod Anim Sust, Campus Realeza, BR-85770000 Realeza - Brazil

^[8] Univ Sao Paulo, Fac Med Vet & Zootecnia, Dept Nutr & Prod Anim, BR-13635900 Pirassununga - Brazil

^[9] Univ Sao Paulo, Fac Med Vet & Zootecnia, Dept Med Vet Prevent & Saude Anim, BR-05508270 Sao Paulo - Brazil

• Document type: Journal article
• Source: JOURNAL OF DAIRY SCIENCE; v. 105, n. 2, p. 1625-1637, FEB 2022.
• Web of Science Citations: 0

Abstract

Mastitis affects a high proportion of dairy cows and is still one of the greatest challenges faced by the dairy industry. Staphylococcal bacteria remain the most important cause of mastitis worldwide. We investigated how distinct staphylococcal species evade some critical host defense mechanisms, which may dictate the establishment, severity, and persistence of infection and the outcome of possible therapeutic and prevention interventions. Thus, the present study investigated variations among distinct bovine-associated staphylococci in their capability to resist phagocytosis and to trigger respiratory burst activity of blood and milk polymorphonuclear neutrophil leukocytes (PMNL) in dairy cows. To do so, PMNL of 6 primiparous and 6 multiparous dairy cows were used. A collection of 38 non-aureus staphylococci (NAS) and 12 Staphylococcus aureus were included. The phagocytosis and intracellular reactive oxygen species (ROS) production by blood and milk PMNL were analyzed by flow cytometry. Phagocytosis, by both blood and milk PMNL, did not differ between S. aureus and NAS as a group, although within-NAS species differences were observed. Staphylococcus chromogenes (a so-called milk-adapted NAS species) better resisted phagocytosis by blood PMNL than the so-called environmental (i.e., Staphylococcus fleurettii) and opportunistic (i.e., Staphylococcus haemolyticus) NAS species. Otherwise, S. haemolyticus was better phagocytosed by blood PMNL than S. aureus, S. fleurettii, and S. chromogenes. No influence of the origin of the isolates within the staphylococci species in the resistance to phagocytosis by blood and milk PMNL was found. Overall, both S. aureus and NAS did not inhibit intracellular ROS production in blood and milk PMNL. Non-aureus staphylococci induced fewer ROS by milk PMNL than S. aureus, which was not true for blood PMNL, although species-specific differences in the intensity of ROS production were observed. Staphylococcus chromogenes induced more blood PMNL ROS than S. fleurettii and S. haemolyticus, and as much as S. aureus. Conversely, S. chromogenes induced fewer milk PMNL ROS than S. aureus. The origin of the isolates within the staphylococci species did not affect the ROS production by blood and milk PMNL. In conclusion, our study showed differences in staphylococci species in evading phagocytosis and triggering ROS production, which may explain the ability of some staphylococci species (i.e., S. aureus and S. chromogenes) to cause persistent infection and induce inflammation. (AU)

• FAPESP's process: 16/06297-3 - Bactericidal killing and phagocytosis by milk phagocytes of distinct bovine-associated staphylococci species and strains in primiparous and multiparous dairy cows
• Grantee: Paula Cristina Cardoso Molinari
• Support Opportunities: Scholarships in Brazil - Scientific Initiation
• FAPESP's process: 17/07921-5 - Crosstalk between mammary epithelial cells and peripheral blood mononuclear cells in intrammary infections by Staphylococcus aureus and by distinct coagulase-negative staphylococci species and strains: development an in vitro model
• Grantee: Fernando Nogueira de Souza
• Support Opportunities: Scholarships abroad - Research Internship - Post-doctor
• FAPESP's process: 18/03685-8 - Impact of teat channel occlusion on the metagenomic profile and its reflex in health of the bovine mammary gland
• Grantee: José Augusto Ferronatto
• Support Opportunities: Scholarships in Brazil - Master
• FAPESP's process: 15/16871-6 - Neutrophil bactericidal killing and phagocytosis of distinct bovine-associated staphylococci species and strains in primiparous and multiparous dairy cows
• Grantee: Alice Maria Melville Paiva Della Libera
• Support Opportunities: Regular Research Grants
• FAPESP's process: 14/23189-4 - Intramammary infections by Staphylococcus aureus: crosstalk between mammary epithelial cells and peripheral blood mononuclear cells, and how it governs immunity in the mammary gland of dairy cows
• Grantee: Fernando Nogueira de Souza
• Support Opportunities: Scholarships in Brazil - Post-Doctoral