Production and release of antimicrobial and immune defense proteins by mammary epithelial cells following Streptococcus uberis infection of sheep

Infection and Immunity

Volumn 81, Issue 9, 2013, Pages 3182-3197

  Addis, Maria Filippa ^a   Pisanu, Salvatore ^a   Marogna, Gavino ^b   Cubeddu, Tiziana ^a,c   Pagnozzi, Daniela ^a   Cacciotto, Carla ^a,c   Campesi, Franca ^c   Schianchi, Giuseppe ^b   Rocca, Stefano ^c   Uzzau, Sergio ^a,c  

^a Porto Conte Ricerche Srl   (Italy)

^b ISTITUTO ZOOPROFILATTICO SPERIMENTALE DELLA SARDEGNA   (Italy)

^c UNIVERSITY OF SASSARI   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CALGRANULIN; CALGRANULIN A; CALGRANULIN B; CATHELICIDIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST EPITHELIUM; CHEMOTAXIS; CONTROLLED STUDY; EPITHELIUM CELL; FLUORESCENCE IN SITU HYBRIDIZATION; IMMUNITY; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INNATE IMMUNITY; INVERSE POLYMERASE CHAIN REACTION; LACTATION; MAMMARY GLAND; MASTITIS; MILK; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SHEEP DISEASE; STREPTOCOCCUS INFECTION; STREPTOCOCCUS UBERIS; WESTERN BLOTTING;

EID: 84884216057     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00291-13     Document Type: Article

References (78)

1. Zadoks RN, Middleton JR, McDougall S, Katholm J, Schukken YH. 2011. Molecular epidemiology of mastitis pathogens of dairy cattle and comparative relevance to humans. J. Mammary Gland Biol. Neoplasia 16:357-372.
2. De Vliegher S, Fox LK, Piepers S, McDougall S, Barkema HW. 2012. Mastitis in dairy heifers: nature of the disease, potential impact, prevention, and control. J. Dairy Sci. 95:1025-1040.
3. Marogna G, Rolesu S, Lollai S, Tola S, Leori S. 2010. Clinical findings in sheep farms affected by recurrent bacterial mastitis. Small Rumin. Res. 88:119-125.
4. Rainard P, Riollet C. 2006. Innate immunity of the bovine mammary gland. Vet. Res. 37:369-400.
5. Beutler B. 2004. Innate immunity: an overview. Mol. Immunol. 40:845-859.
6. Zecconi A, Hamann J, Bronzo V, Moroni P, Giovannini G, Piccinini R. 2000. Relationship between teat tissue immune defences and intramammary infections, Adv. Exp. Med. Biol. 480:287-293.
7. Schultze WD, Bright SC. 1983. Changes in penetrability of bovine papillary duct to endotoxin after milking. Am. J. Vet. Res. 44:2373-2375.
8. McDougall S, Lopez-Villalobos N, Prosser CG. 2011. Relationship between estimated breeding value for somatic cell count and prevalence of intramammary infection in dairy goats. N. Z. Vet. J. 59:300-304.
9. Middleton JR, Hardin D, Steevens B, Randle R, Tyler JW. 2004. Use of somatic cell counts and California mastitis test results from individual quarter milk samples to detect subclinical intramammary infection in dairy cattle from a herd with a high bulk tank somatic cell count. J. Am. Vet. Med. Assoc. 224:419-423.
10. De Haas Y, Veerkamp RF, Barkema HW, Gröhn YT, Schukken YH. 2004. Associations between pathogen-specific cases of clinical mastitis and somatic cell count patterns. J. Dairy Sci. 87:95-105.
11. McDougall S, Murdough P, Pankey W, Delaney C, Barlow J, Scruton D. 2001. Relationships among somatic cell count, California mastitis test, impedance and bacteriological status of milk in goats and sheep in early lactation. Small Rumin. Res. 40:245-254.
12. Ryan DP, Greenwood PL, Nicholls PJ. 1993. Effect of caprine arthritisencephalitis virus infection on milk cell count and N-acetyl-betaglucosaminidase activity in dairy goats. J. Dairy Res. 60:299-306.
13. Pekelder JJ, Veenink GJ, Akkermans JP, van Eldik P, Elving L, Houwers DJ. 1994. Ovine lentivirus induced indurative lymphocytic mastitis and its effect on the growth of lambs. Vet. Rec. 134:348-350.
14. Lerondelle C, Richard Y, Issartial J. 1992. Factors affecting somatic cell counts in goat milk. Small Rumin. Res. 8:129-139.
15. Gonzalo C, Carriedo JA, Baro JA, San Primitivo F. 1994. Factors influencing variation of test day milk yield, somatic cell count, fat, and protein in dairy sheep. J. Dairy Sci. 77:1537-1542.
16. Gonzalo C, Carriedo JA, García-Jimeno MC, Pérez-Bilbao M, de la Fuente LF. 2010. Factors influencing variation of bulk milk antibiotic residue occurrence, somatic cell count, and total bacterial count in dairy sheep flocks. J. Dairy Sci. 93:1587-1595.
17. Zeng SS, Escobar EN, Popham T. 1997. Daily variations in somatic cell count, composition, and production of alpine goat milk. Small Rumin. Res. 26:253-260.
18. Addis MF, Pisanu S, Ghisaura S, Pagnozzi D, Marogna G, Tanca A, Biosa G, Cacciotto C, Alberti A, Pittau M, Roggio T, Uzzau S. 2011. Proteomics and pathway analyses of the milk fat globule in sheep naturally infected by Mycoplasma agalactiae provide indications of the in vivo response of the mammary epithelium to bacterial infection. Infect. Immun. 79:3833-3845.
19. Almeida RA, Gillespie BE, Lewis MJ, Headrick SJ, Oliver SP. 2004. Development of an experimental Streptococcus uberis intramammary infection model, p 282-283. In Annual meeting-National Mastitis Council Incorporated. Proceedings of the 43rd Annual Meeting of the National Mastitis Council.
20. Pedersen L, Aalbaek B, Rontved C, Ingvarstsen K, Sorensen N, Heegaard P, Jensen H. 2003. Early pathogenesis and inflammatory response in experimental bovine mastitis due to Streptococcus uberis. J. Comp. Pathol. 128:156-164.
21. Rambeaud M, Almeida R, Pighetti G, Oliver S. 2003. Dynamics of leukocytes and cytokines during experimentally induced Streptococcus uberis mastitis. Vet. Immunol. Immunopathol. 96:193-205.
22. Schnare M, Barton GM, Holt AC, Takeda K, Akira S, Medzhitov R. 2001. Toll-like receptors control activation of adaptive immune responses. Nat. Immunol. 2:947-950.
23. Akira S, Uematsu S, Takeuchi O. 2006. Pathogen recognition and innate immunity. Cell 124:783-801.
24. Schukken YH, Günther J, Fitzpatrick J, Fontaine MC, Goetze L, Holst O, Leigh J, Petzl W, Schuberth HJ, Sipka A, Smith DG, Quesnell R, Watts J, Yancey R, Zerbe H, Gurjar A, Zadoks RN, Seyfert HM. 2011. Host-response patterns of intramammary infections in dairy cows. Vet. Immunol. Immunopathol. 144:270-289.
25. Van Wetering S, Tjabringa GS, Hiemstra PS. 2005. Interactions between neutrophil-derived antimicrobial peptides and airway epithelial cells. J. Leukoc. Biol. 77:444-450.
26. Bowdish DM, Davidson DJ, Lau YE, Lee K, Scott MG, Hancock RE. 2005. Impact of LL-37 on anti-infective immunity. J. Leukoc. Biol. 77:451-459.
27. Akerstedt M, Waller KP, Sternesjö A. 2009. Haptoglobin and serum amyloid A in bulk tank milk in relation to raw milk quality. J. Dairy Res. 76:483-489.
28. Eckersall PD. 2004. The time is right for acute phase proteins assay. Vet. J. 168:3-5.
29. Eckersall PD, Young FJ, Nolan AM, Knight CH, McComb C, Waterston MM, Hogarth CJ, Scott EM, Fitzpatrick JL. 2006. Acute phase proteins in bovine milk in an experimental model of Staphylococcus aureus subclinical mastitis. J. Dairy Sci. 89:1488-1501.
30. Downing TE, Sporn TA, Bollinger RR, Davis RD, Parker W, Lin SS. 2008. Pulmonary histopathology in an experimental model of chronic aspiration is independent of acidity. Exp. Biol. Med. (Maywood) 233:1202-1212.
31. Pisanu S, Ghisaura S, Pagnozzi D, Biosa G, Tanca A, Roggio T, Uzzau S, Addis MF. 2011. The sheep milk fat globule membrane proteome. J. Proteomics 74:350-358.
32. Pisanu S, Ghisaura S, Pagnozzi D, Falchi G, Biosa G, Tanca A, Roggio T, Uzzau S, Addis MF. 2012. Characterization of sheep milk fat globule proteins by two-dimensional polyacrylamide gel electrophoresis/mass spectrometry and generation of a reference map. Int. Dairy J. 24:78-86.
33. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
34. Terova G, Addis MF, Preziosa E, Pisanu S, Pagnozzi D, Biosa G, Gornati R, Bernardini G, Roggio T, Saroglia M. 2011. Effects of postmortem storage temperature on sea bass (Dicentrarchus labrax) muscle protein degradation: analysis by 2-D DIGE and MS. Proteomics 11:2901-2910.
35. Tanca A, Biosa G, Pagnozzi D, Addis MF, Uzzau S. 2013. Comparison of detergent-based sample preparation workflows for LTQ-Orbitrap analysis of the Escherichia coli proteome. Proteomics doi:10.1002/pmic.201200478.
36. Spivak M, Weston J, Bottou L, Kall L, Noble WS. 2009. Improvements to the percolator algorithm for peptide identification from shotgun proteomics data sets. J. Proteome Res. 8:3737-3745.
37. Old WM, Meyer-Arendt K, Aveline-Wolf L, Pierce KG, Mendoza A, Sevinsky JR, Resing KA, Ahn NG. 2005. Comparison of label-free methods for quantifying human proteins by shotgun proteomics. Mol. Cell. Proteomics 4:1487-1502.
38. Zybailov B, Mosley AL, Sardiu ME, Coleman MK, Florens L, Washburn MP. 2006. Statistical analysis of membrane proteome expression changes in Saccharomyces cerevisiae. J. Proteome Res. 5:2339-2347.
39. Pham TV, Piersma SR, Warmoes M, Jimenez CR. 2010. On the betabinomial model for analysis of spectral count data in label-free tandem mass spectrometry based proteomics. Bioinformatics 26:363-369.
40. Mitterhuemer S, Petzl W, Krebs S, Mehne D, Klanner A, Wolf E, Zerbe H, Blum H. 2010. Escherichia coli infection induces distinct local and systemic transcriptome responses in the mammary gland. BMC Genomics 11:138. doi:10.1186/1471-2164-11-138.
41. Lasagno MC, Vissio C, Reinoso EB, Raspanti C, Yaciuk R, Larriestra AJ, Odierno LM. 2012. Development of an experimentally induced Streptococcus uberis subclinical mastitis in goats. Vet. Microbiol. 154:376-383.
42. Dopfer D, Barkema HW, Lam TJ, Schukken YH, Gaastra W. 1999. Recurrent clinical mastitis caused by Escherichia coli in dairy cows. J. Dairy Sci. 82:80-85.
43. Brenaut P, Bangera R, Bevilacqua C, Rebours E, Cebo C, Martin P. 2012. Validation of RNA isolated from milk fat globules to profile mammary epithelial cell expression during lactation and transcriptional response to a bacterial infection. J. Dairy Sci. 95:6130-6144.
44. Heid HW, Keenan TW. 2005. Intracellular origin and secretion of milk fat globules. Eur. J. Cell Biol. 84:245-258.
45. Pisanu S, Marogna G, Pagnozzi D, Piccinini M, Leo G, Tanca A, Roggio AM, Roggio T, Uzzau S, Addis MF. 2012. Characterization of size and composition of milk fat globules from Sarda and Saanen dairy goats. Small Rumin. Res. 109:141-151.
46. Cebo C, Caillat H, Bouvier P, Martin P. 2010. Major proteins of the goat milk fat globule membrane. J. Dairy Sci. 93:868-876.
47. Harmon RJ, Newbould FHS. 1980. Neutrophil leukocyte as a source of lactoferrin in bovine milk. Am. J. Vet. Res. 41:1603-1606.
48. Legrand D, Elass E, Pierce A, Mazurier J. 2004. Lactoferrin and host defence: an overview of its immuno-modulating and anti-inflammatory properties. Biometals 17:225-229.
49. Brock J. 1995. Lactoferrin: a multifunctional immunoregulatory protein? Immunol. Today 16:417-419.
50. Petersen HH, Nielsen JP, Heegaard PM. 2004. Application of acute phase protein measurements in veterinary clinical chemistry. Vet. Res. 35:163-187.
51. Wellnitz O, Kerr DE. 2004. Cryopreserved bovine mammary cells to model epithelial response to infection. Vet. Immunol. Immunopathol. 101:191-202.
52. Lai IH, Tsao JH, Lu YP, Lee JW, Zhao X, Chien FL, Mao SJ. 2009. Neutrophils as one of the major haptoglobin sources in mastitis affected milk. Vet. Res. 40:17.
53. Bargagli E, Olivieri C, Prasse A, Bianchi N, Magi B, Cianti R, Bini L, Rottoli P. 2008. Calgranulin B (S100A9) levels in bronchoalveolar lavage fluid of patients with interstitial lung diseases. Inflammation 31:351-354.
54. Striz I, Trebichavsky I. 2004. Calprotectin: a pleiotropic molecule in acute and chronic inflammation. Physiol. Res. 53:245-253.
55. Barthe C, Figarella C, Carrere J, Guy-Crotte O. 1991. Identification of "cystic fibrosis protein" as a complex of two calcium-binding proteins present in human cells of myeloid origin. Biochim. Biophys. Acta 1096:175-177.
56. Berntzen HB, Olmez U, Fagerhol MK, Munthe E. 1991. The leukocyte protein L1 in plasma and synovial fluid from patients with rheumatoid arthritis and osteoarthritis. Scand. J. Rheumatol. 20:74-82.
57. Hu SP, Harrison C, Xu K, Cornish CJ, Geczy CL. 1996. Induction of the chemotactic S100 protein, CP-10, in monocyte/macrophages by lipopolysaccharide. Blood 87:3919-3928.
58. Lusitani D, Malawista SE, Montgomery RR. 2003. Calprotectin, an abundant cytosolic protein from human polymorphonuclear leukocytes, inhibits the growth of Borrelia burgdorferi. Infect. Immun. 71:4711-4716.
59. Liu JZ, Jellbauer S, Poe AJ, Ton V, Pesciaroli M, Kehl-Fie TE, Restrepo NA, Hosking MP, Edwards RA, Battistoni A, Pasquali P, Lane TE, Chazin WJ, Vogl T, Roth J, Skaar EP, Raffatellu M. 2012. Zinc sequestration by the neutrophil protein calprotectin enhances Salmonella growth in the inflamed gut. Cell Host Microbe 11:227-239.
60. Raquil MA, Anceriz N, Rouleau P, Tessier PA. 2008. Blockade of antimicrobial proteins S100A8 and S100A9 inhibits phagocyte migration to the alveoli in streptococcal pneumonia. J. Immunol. 180:3366-3374.
61. Ryckman C, Vandal K, Rouleau P, Talbot M, Tessier PA. 2003. Proinflammatory activities of S100: proteins S100A8, S100A9, and S100A8/A9 induce neutrophil chemotaxis and adhesion. J. Immunol. 170:3233-3242.
62. Vandal K, Rouleau P, Boivin A, Ryckman C, Talbot M, Tessier PA. 2003. Blockade of S100A8 and S100A9 suppresses neutrophil migration in response to lipopolysaccharide. J. Immunol. 171:2602-2609.
63. Corbin BD, Seeley EH, Raab A, Feldmann J, Miller MR, Torres VJ, Anderson KL, Dattilo BM, Dunman PM, Gerads R, Caprioli RM, Nacken W, Chazin WJ, Skaar EP. 2008. Metal chelation and inhibition of bacterial growth in tissue abscesses. Science 319:962-965.
64. Damo SM, Kehl-Fie TE, Sugitani N, Holt ME, Rathi S, Murphy WJ, Zhang Y, Betz C, Hench L, Fritz G, Skaar EP, Chazin WJ. 2013. Molecular basis for manganese sequestration by calprotectin and roles in the innate immune response to invading bacterial pathogens. Proc. Natl. Acad. Sci. U. S. A. 110:3841-3846.
65. Hayden JA, Brophy MB, Cunden LS, Nolan EM. 2013. High-affinity manganese coordination by human calprotectin is calcium-dependent and requires the histidine-rich site formed at the dimer interface. J. Am. Chem. Soc. 135:775-787.
66. Urban CF, Ermert D, Schmid M, Abu-Abed U, Goosmann C, Nacken W, Brinkmann V, Jungblut PR, Zychlinsky A. 2009. Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog. 5:e1000639. doi:10.1371/journal.ppat.1000639.
67. Chromek M, Slamová Z, Bergman P, Kovács L, Podracká L, Ehrén I, Hökfelt T, Gudmundsson GH, Gallo RL, Agerberth B, Brauner A. 2006. The antimicrobial peptide cathelicidin protects the urinary tract against invasive bacterial infection. Nat. Med. 12:636-641.
68. Wiesner J, Vilcinskas A. 2010. Antimicrobial peptides: the ancient arm of the human immune system. Virulence 1:440-464.
69. Zanetti M. 2004. Cathelicidins, multifunctional peptides of the innate immunity. J. Leukoc. Biol. 75:39-48.
70. Boman HG. 2003. Antibacterial peptides: basic facts and emerging concepts. J. Intern. Med. 254:197-215.
71. Zaiou M, Nizet V, Gallo RL. 2003. Antimicrobial and protease inhibitory functions of the human cathelicidin (hCAP18/LL-37) prosequence. J. Investig. Dermatol. 120:810-816.
72. Sørensen OE, Follin P, Johnsen AH, Calafat J, Tjabringa GS, Hiemstra PS, Borregaard N. 2001. Human cathelicidin, hCAP-18, is processed to the antimicrobial peptide LL-37 by extracellular cleavage with proteinase 3. Blood 97:3951-3959.
73. Zanetti M. 2005. The role of cathelicidins in the innate host defenses of mammals. Curr. Issues Mol. Biol. 7:179-196.
74. Nijnik A, Hancock RE. 2009. The roles of cathelicidin LL-37 in immune defences and novel clinical applications. Curr. Opin. Hematol. 16:41-47.
75. Tomasinsig L, De Conti G, Skerlavaj B, Piccinini R, Mazzilli M, D'Este F, Tossi A, Zanetti M. 2010. Broad-spectrum activity against bacterial mastitis pathogens and activation of mammary epithelial cells support a protective role of neutrophil cathelicidins in bovine mastitis. Infect. Immun. 78:1781-1788.
76. Ibeagha-Awemu EM, Ibeagha AE, Messier S, Zhao X. 2010. Proteomics, genomics, and pathway analyses of Escherichia coli and Staphylococcus aureus infected milk whey reveal molecular pathways and networks involved in mastitis. J. Proteome Res. 9:4604-4619.
77. Reinhardt TA, Sacco RE, Nonnecke BJ, Lippolis JD. 2013. Bovine milk proteome: quantitative changes in normal milk exosomes, milk fat globule membranes and whey proteomes resulting from Staphylococcus aureus mastitis. J. Proteomics 82:141-154.
78. Smolenski GA, Wieliczko RJ, Pryor SM, Broadhurst MK, Wheeler TT, Haigh BJ. 2011. The abundance of milk cathelicidin proteins during bovine mastitis. Vet. Immunol. Immunopathol. 143:125-130.