Treating canine atopic dermatitis with unsaturated fatty acids: The role of mast cells and potential mechanisms of action

Journal of Animal Physiology and Animal Nutrition

Volumn 98, Issue 6, 2014, Pages 1013-1020

  Schumann, J ^a   Basiouni, S ^a,b   Guck T ^c   Fuhrmann, H ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b Benha University   (Egypt)

^c Hill's Pet Nutrition GmbH   (Germany)

Author keywords

Canine atopic dermatitis; Lipid rafts; Mast cells; Phospholipases d; Polyunsaturated fatty acids

Indexed keywords

CANIS FAMILIARIS;

UNSATURATED FATTY ACID;

ANIMAL; ANIMAL FOOD; DERMATITIS, ATOPIC; DIET SUPPLEMENTATION; DOG; DOG DISEASES; DRUG EFFECTS; MAST CELL; METABOLISM; VETERINARY;

ANIMAL FEED; ANIMALS; DERMATITIS, ATOPIC; DIETARY SUPPLEMENTS; DOG DISEASES; DOGS; FATTY ACIDS, UNSATURATED; MAST CELLS;

EID: 84920420778     PISSN: 09312439     EISSN: 14390396     Source Type: Journal    
DOI: 10.1111/jpn.12181     Document Type: Review

References (86)

1. Araki, S.; Ito, M.; Kureishi, Y.; Feng, J.; Machida, H.; Isaka, N.; Amano, M.; Kaibuchi, K.; Hartshorne, D. J.; Nakano, T., 2001: Arachidonic acid-induced Ca2+ sensitization of smooth muscle contraction through activation of Rho-kinase. Pflugers Archiv 441, 596-603.
2. Askari, B.; Carroll, M. A.; Capparelli, M.; Kramer, F.; Gerrity, R. G.; Bornfeldt, K. E., 2002: Oleate and linoleate enhance the growth-promoting effects of insulin-like growth factor-I through a phospholipase D-dependent pathway in arterial smooth muscle cells. Journal of Biological Chemistry 277, 36338-36344.
3. Auxilia, S. T.; Hill, P. B., 2000: Mast cell distribution, epidermal thickness and hair follicle density in normal canine skin: possible explanations for the predilection sites of atopic dermatitis? Veterinary Dermatology 11, 247-254.
4. Awad, A. B.; Basilious, B. G.; Fink, C. S.; Horvath, P. J., 1994: In vitro activation and inhibition of rat colonic phospholipase D by fatty acids. Cancer Letters 86, 105-109.
5. Basiouni, S.; Stockel, K.; Fuhrmann, H.; Schumann, J., 2012: Polyunsaturated fatty acid supplements modulate mast cell membrane microdomain composition. Cellular Immunology 275, 42-46.
6. Basiouni, S.; Fuhrmann, H.; Schumann, J., 2013: The influence of polyunsaturated fatty acids on the phospholipase d isoforms trafficking and activity in mast cells. International Journal of Molecular Sciences 14, 9005-9017.
7. Baumer, W.; Stahl, J.; Sander, K.; Petersen, L. J.; Paps, J.; Stark, H.; Kietzmann, M.; Olivry, T., 2011: Lack of preventing effect of systemically and topically administered histamine H(1) or H(4) receptor antagonists in a dog model of acute atopic dermatitis. Experimental Dermatology 20, 577-581.
8. Bechoua, S.; Dubois, M.; Nemoz, G.; Lagarde, M.; Prigent, A. F., 1998: Docosahexaenoic acid lowers phosphatidate level in human activated lymphocytes despite phospholipase D activation. Journal of Lipid Research 39, 873-883.
9. Bensignor, E.; Morgan, D. M.; Nuttall, T., 2008: Efficacy of an essential fatty acid-enriched diet in managing canine atopic dermatitis: a randomized, single-blinded, cross-over study. Veterinary Dermatology 19, 156-162.
10. Biondo, P. D.; Brindley, D. N.; Sawyer, M. B.; Field, C. J., 2008: The potential for treatment with dietary long-chain polyunsaturated n-3 fatty acids during chemotherapy. Journal of Nutritional Biochemistry 19, 787-796.
11. Boyce, J. A., 2007: Mast cells and eicosanoid mediators: a system of reciprocal paracrine and autocrine regulation. Immunological Reviews 217, 168-185.
12. Brown, F. D.; Thompson, N.; Saqib, K. M.; Clark, J. M.; Powner, D.; Thompson, N. T.; Solari, R.; Wakelam, M. J., 1998: Phospholipase D1 localises to secretory granules and lysosomes and is plasma-membrane translocated on cellular stimulation. Current Biology 8, 835-838.
13. Burr, G. O.; Burr, M. M., 1929: A new deficiency disease produced by the rigid exclusion of fat from the diet. Journal of Biological Chemistry 82, 345-367.
14. Burr, G. O.; Burr, M. M., 1930: On the nature and the role of the fatty acids essential in nutrition. Journal of Biological Chemistry 86, 587-621.
15. Carr, M. N.; Torres, S. M.; Koch, S. N.; Reiter, L. V., 2009: Investigation of the pruritogenic effects of histamine, serotonin, tryptase, substance P and interleukin-2 in healthy dogs. Veterinary Dermatology 20, 105-110.
16. Choi, W. S.; Kim, Y. M.; Combs, C.; Frohman, M. A.; Beaven, M. A., 2002: Phospholipases D1 and D2 regulate different phases of exocytosis in mast cells. Journal of Immunology 168, 5682-5689.
17. Colley, W. C.; Sung, T. C.; Roll, R.; Jenco, J.; Hammond, S. M.; Altshuller, Y.; Bar-Sagi, D.; Morris, A. J.; Frohman, M. A., 1997: Phospholipase D2, a distinct phospholipase D isoform with novel regulatory properties that provokes cytoskeletal reorganization. Current Biology 7, 191-201.
18. Davey, A. M.; Walvick, R. P.; Liu, Y.; Heikal, A. A.; Sheets, E. D., 2007: Membrane order and molecular dynamics associated with IgE receptor cross-linking in mast cells. Biophysical Journal 92, 343-355.
19. Davey, A. M.; Krise, K. M.; Sheets, E. D.; Heikal, A. A., 2008: Molecular perspective of antigen-mediated mast cell signaling. Journal of Biological Chemistry 283, 7117-7127.
20. DeMora, F.; Garcia, G.; Puigdemont, A.; Arboix, M.; Ferrer, L., 1996: Skin mast cell releasability in dogs with atopic dermatitis. Inflammation Research 45, 424-427.
21. Denys, A.; Hichami, A.; Khan, N. A., 2005: n-3 PUFAs modulate T-cell activation via protein kinase C-alpha and -epsilon and the NF-kappaB signaling pathway. Journal of Lipid Research 46, 752-758.
22. Diaz, O.; Berquand, A.; Dubois, M.; Di, A. S.; Sette, C.; Bourgoin, S.; Lagarde, M.; Nemoz, G.; Prigent, A. F., 2002: The mechanism of docosahexaenoic acid-induced phospholipase D activation in human lymphocytes involves exclusion of the enzyme from lipid rafts. Journal of Biological Chemistry 277, 39368-39378.
23. Epand, R. M., 1998: Lipid polymorphism and protein-lipid interactions. Biochimica et Biophysica Acta 1376, 353-368.
24. Fu, X.; Gong, M. C.; Jia, T.; Somlyo, A. V.; Somlyo, A. P., 1998: The effects of the Rho-kinase inhibitor Y-27632 on arachidonic acid-, GTPgammaS-, and phorbol ester-induced Ca2+-sensitization of smooth muscle. FEBS Letters 440, 183-187.
25. Fuhrmann, H.; Zimmermann, A.; Guck, T.; Oechtering, G., 2006: Erythrocyte and plasma fatty acid patterns in dogs with atopic dermatitis and healthy dogs in the same household. Canadian Journal of Veterinary Research 70, 191-196.
26. Fujii, M.; Nakashima, H.; Tomozawa, J.; Shimazaki, Y.; Ohyanagi, C.; Kawaguchi, N.; Ohya, S.; Kohno, S.; Nabe, T., 2013: Deficiency of n-6 polyunsaturated fatty acids is mainly responsible for atopic dermatitis-like pruritic skin inflammation in special diet-fed hairless mice. Experimental Dermatology 22, 272-277.
27. Garbi, M.; Rubinstein, S.; Lax, Y.; Breitbart, H., 2000: Activation of protein kinase calpha in the lysophosphatidic acid-induced bovine sperm acrosome reaction and phospholipase D1 regulation. Biology of Reproduction 63, 1271-1277.
28. Gemeinhardt, A.; Alfalah, M.; Guck, T.; Naim, H. Y.; Fuhrmann, H., 2009: The influence of linoleic and linolenic acid on the activity and intracellular localisation of phospholipase D in COS-1 cells. Biological Chemistry 390, 253-258.
29. Grenier, S.; Flamand, N.; Pelletier, J.; Naccache, P. H.; Borgeat, P.; Bourgoin, S. G., 2003: Arachidonic acid activates phospholipase D in human neutrophils; essential role of endogenous leukotriene B4 and inhibition by adenosine A2A receptor engagement. Journal of Leukocyte Biology 73, 530-539.
30. Griffin, C. E.; DeBoer, D. J., 2001: The ACVD task force on canine atopic dermatitis (XIV): clinical manifestations of canine atopic dermatitis. Veterinary Immunology and Immunopathology 81, 255-269.
31. Gueck, T.; Seidel, A.; Fuhrmann, H., 2003: Effects of essential fatty acids on mediators of mast cells in culture. Prostaglandins Leukotrienes and Essential Fatty Acids 68, 317-322.
32. Gueck, T.; Seidel, A.; Baumann, D.; Meister, A.; Fuhrmann, H., 2004a: Alterations of mast cell mediator production and release by gamma-linolenic and docosahexaenoic acid. Veterinary Dermatology 15, 309-314.
33. Gueck, T.; Seidel, A.; Fuhrmann, H., 2004b: Consequences of eicosapentaenoic acid (n-3) and arachidonic acid (n-6) supplementation on mast cell mediators. Journal of Animal Physiology and Animal Nutrition 88, 259-265.
34. Halliwell, R. E.; Schwartzman, R. M., 1971: Atopic disease in dog. Veterinary Record 89, 209-214.
35. Harvey, R. G., 1999: A blinded, placebo-controlled study of the efficacy of borage seed oil and fish oil in the management of canine atopy. Veterinary Record 144, 405-407.
36. Hill, P. B.; Olivry, T., 2001: The ACVD task force on canine atopic dermatitis (V): biology and role of inflammatory cells in cutaneous allergic reactions. Veterinary Immunology and Immunopathology 81, 187-198.
37. Hill, P. B.; Hillier, A.; Olivry, T., 2001: The ACVD task force on canine atopic dermatitis (VI): IgE-induced immediate and late-phase reactions, two inflammatory sequences at sites of intradermal allergen injections. Veterinary Immunology and Immunopathology 81, 199-204.
38. Hillier, A.; Griffin, C. E., 2001: The ACVD task force on canine atopic dermatitis (I): incidence and prevalence. Veterinary Immunology and Immunopathology 81, 147-151.
39. Hu, T.; Exton, J. H., 2003: Mechanisms of regulation of phospholipase D1 by protein kinase Calpha. Journal of Biological Chemistry 278, 2348-2355.
40. Hunter, M. J.; Iodice, M. W.; Pathak, A. K.; Street, M. A.; Helm, B. A., 2009: Characterization of an early signaling defect following Fc epsilonRI activation in the canine mastocytoma cell line, C2. Molecular Immunology 46, 1260-1265.
41. Jakobsson, A.; Westerberg, R.; Jacobsson, A., 2006: Fatty acid elongases in mammals: their regulation and roles in metabolism. Progress in Lipid Research 45, 237-249.
42. Khan, W. A.; Blobe, G. C.; Hannun, Y. A., 1995: Arachidonic acid and free fatty acids as second messengers and the role of protein kinase C. Cellular Signaling 7, 171-184.
43. Kim, J. H.; Kim, Y.; Lee, S. D.; Lopez, I.; Arnold, R. S.; Lambeth, J. D.; Suh, P. G.; Ryu, S. H., 1999: Selective activation of phospholipase D2 by unsaturated fatty acid. FEBS Letters 454, 42-46.
44. Koenig, B. W.; Strey, H. H.; Gawrisch, K., 1997: Membrane lateral compressibility determined by NMR and x-ray diffraction: effect of acyl chain polyunsaturation. Biophysical Journal 73, 1954-1966.
45. Lauber, B.; Molitor, V.; Meury, S.; Doherr, M. G.; Favrot, C.; Tengvall, K.; Bergvall, K.; Leeb, T.; Roosje, P.; Marti, E., 2012: Total IgE and allergen-specific IgE and IgG antibody levels in sera of atopic dermatitis affected and non-affected Labrador- and Golden retrievers. Veterinary Immunology and Immunopathology 149, 112-118.
46. Loewenstein, C.; Mueller, R. S., 2009: A review of allergen-specific immunotherapy in human and veterinary medicine. Veterinary Dermatology 20, 84-98.
47. Lopez-Nicolas, R.; Lopez-Andreo, M. J.; Marin-Vicente, C.; Gomez-Fernandez, J. C.; Corbalan-Garcia, S., 2006: Molecular mechanisms of PKCalpha localization and activation by arachidonic acid. The C2 domain also plays a role. Journal of Molecular Biology 357, 1105-1120.
48. Ma, D. W. L.; Seo, J.; Switzer, K. C.; Fan, Y. Y.; McMurray, D. N.; Lupton, J. R.; Chapkin, R. S., 2004: n-3 PUFA and membrane microdomains: a new frontier in bioactive lipid research. Journal of Nutritional Biochemistry 15, 700-706.
49. Marsella, R.; Olivry, T., 2001: The ACVD task force on canine atopic dermatitis (VII): mediators of cutaneous inflammation. Veterinary Immunology and Immunopathology 81, 205-213.
50. Marsh, K. A.; Ruedisueli, F. L.; Coe, S. L.; Watson, T. D. G., 2000: Effects of zinc and linoleic acid supplementation on the skin and coat quality of dogs receiving a complete and balanced diet. Veterinary Dermatology 11, 277-284.
51. Mochly-Rosen, D.; Henrich, C. J.; Cheever, L.; Khaner, H.; Simpson, P. C., 1990: A protein kinase C isozyme is translocated to cytoskeletal elements on activation. Cell Regulation 1, 693-706.
52. Nair, S. S.; Leitch, J.; Garg, M. L., 2001: N-3 polyunsaturated fatty acid supplementation alters inositol phosphate metabolism and protein kinase C activity in adult porcine cardiac myocytes. Journal of Nutritional Biochemistry 12, 7-13.
53. Olivry, T., 2011: Is the skin barrier abnormal in dogs with atopic dermatitis? Veterinary Immunology and Immunopathology 144, 11-16.
54. Olivry, T.; Bizikova, P., 2013: A systematic review of randomized controlled trials for prevention or treatment of atopic dermatitis in dogs: 2008-2011 update. Veterinary Dermatology 24, 97-117.
55. Olivry, T.; Hill, P. B., 2001: The ACVD task force on canine atopic dermatitis (VIII): is the epidermal lipid barrier defective? Veterinary Immunology and Immunopathology 81, 215-218.
56. Olivry, T.; Sousa, C. A., 2001: The ACVD task force on canine atopic dermatitis (XIX): general principles of therapy. Veterinary Immunology and Immunopathology 81, 311-316.
57. Olivry, T.; Marsella, R.; Hillier, A., 2001: The ACVD task force on canine atopic dermatitis (XXIII): are essential fatty acids effective? Veterinary Immunology and Immunopathology 81, 347-362.
58. Olivry, T.; DeBoer, D. J.; Favrot, C.; Jackson, H. A.; Mueller, R. S.; Nuttall, T.; Prelaud, P., 2010a: Treatment of canine atopic dermatitis: 2010 clinical practice guidelines from the International Task Force on Canine Atopic Dermatitis. Veterinary Dermatology 21, 233-248.
59. Olivry, T.; Foster, A. P.; Mueller, R. S.; McEwan, N. A.; Chesney, C.; Williams, H. C., 2010b: Interventions for atopic dermatitis in dogs: a systematic review of randomized controlled trials. Veterinary Dermatology 21, 4-22.
60. Pejler, G.; Ronnberg, E.; Waern, I.; Wernersson, S., 2010: Mast cell proteases: multifaceted regulators of inflammatory disease. Blood 115, 4981-4990.
61. Peng, X.; Frohman, M. A., 2012: Mammalian phospholipase D physiological and pathological roles. Acta Physiologica 204, 219-226.
62. Pike, L. J., 2003: Lipid rafts: bringing order to chaos. Journal of Lipid Research 44, 655-667.
63. Rees, C. A.; Bauer, J. E.; Burkholder, W. J.; Kennis, R. A.; Dunbar, B. L.; Bigley, K. E., 2001: Effects of dietary flax seed and sunflower seed supplementation on normal canine serum polyunsaturated fatty acids and skin and hair coat condition scores. Veterinary Dermatology 12, 111-117.
64. Rossbach, K.; Stark, H.; Sander, K.; Leurs, R.; Kietzmann, M.; Baumer, W., 2009: The histamine H receptor as a new target for treatment of canine inflammatory skin diseases. Veterinary Dermatology 20, 555-561.
65. Saevik, B. K.; Bergvall, K.; Holm, B. R.; Saijonmaa-Koulumies, L. E.; Hedhammar, A.; Larsen, S.; Kristensen, F., 2004: A randomized, controlled study to evaluate the steroid sparing effect of essential fatty acid supplementation in the treatment of canine atopic dermatitis. Veterinary Dermatology 15, 137-145.
66. Schlotter, Y. M.; Veenhof, E. Z.; Brinkhof, B.; Rutten, V. P.; Spee, B.; Willemse, T.; Penning, L. C., 2009: A GeNorm algorithm-based selection of reference genes for quantitative real-time PCR in skin biopsies of healthy dogs and dogs with atopic dermatitis. Veterinary Immunology and Immunopathology 129, 115-118.
67. Schmitz, G.; Grandl, M., 2008: Update on lipid membrane microdomains. Current Opinion in Clinical Nutrition and Metabolic Care 11, 106-112.
68. Schmutzler, S.; Bachmann, L.; Fuhrmann, H.; Schumann, J., 2010: PUFA-dependent alteration of oxidative parameters of a canine mastocytoma cell line. Acta Veterinaria Hungarica 58, 453-464.
69. Scott, D. W.; Miller, W. H. Jr; Reinhart, G. A.; Mohammed, H. O.; Bagladi, M. S., 1997: Effect of an omega-3/omega-6 fatty acid-containing commercial lamb and rice diet on pruritus in atopic dogs: results of a single-blinded study. Canadian Journal of Veterinary Research 61, 145-153.
70. Seidel, A.; Gueck, T.; Fuhrmann, H., 2005: The Influence of long-chain polyunsaturated fatty acids on total lipid fatty acid composition of a canine mastocytoma cell line. Journal of Veterinary Medicine Series A - Physiology, Pathology, Clinical Medicine 52, 219-224.
71. Selvy, P. E.; Lavieri, R. R.; Lindsley, C. W.; Brown, H. A., 2011: Phospholipase D: enzymology, functionality, and chemical modulation. Chemical Reviews 111, 6064-6119.
72. Siddiqui, R. A.; Harvey, K. A.; Zaloga, G. P.; Stillwell, W., 2007: Modulation of lipid rafts by Omega-3 fatty acids in inflammation and cancer: implications for use of lipids during nutrition support. Nutrition in Clinical Practice 22, 74-88.
73. Simons, K.; Toomre, D., 2000: Lipid rafts and signal transduction. Nature Reviews Molecular Cell Biology 1, 31-39.
74. Smaby, J. M.; Momsen, M. M.; Brockman, H. L.; Brown, R. E., 1997: Phosphatidylcholine acyl unsaturation modulates the decrease in interfacial elasticity induced by cholesterol. Biophysical. Journal 73, 1492-1505.
75. Sprecher, H.; Luthria, D. L.; Mohammed, B. S.; Baykousheva, S. P., 1995: Reevaluation of the pathways for the biosynthesis of polyunsaturated fatty acids. Journal of Lipid Research 36, 2471-2477.
76. Stillwell, W.; Wassall, S. R., 2003: Docosahexaenoic acid: membrane properties of a unique fatty acid. Chemistry and Physics of Lipids 126, 1-27.
77. Stoeckel, K.; Nielsen, L. H.; Fuhrmann, H.; Bachmann, L., 2011: Fatty acid patterns of dog erythrocyte membranes after feeding of a fish-oil based DHA-rich supplement with a base diet low in n-3 fatty acids versus a diet containing added n-3 fatty acids. Acta Veterinaria Scandinavica 53, 57.
78. Stoeckel, K.; Bachmann, L.; Dobeleit, G.; Fuhrmann, H., 2012: Response of plasma fatty acid profiles to changes in dietary n-3 fatty acids and its correlation with erythrocyte fatty acid profiles in dogs. Journal of Animal Physiology and Animal Nutrition 97, 1142-1151.
79. Van Laethem, F.; Leo, O., 2002: Membrane lipid rafts: new targets for immunoregulation. Current Molecular Medicine 2, 557-570.
80. Vaughn, D. M.; Reinhart, G. A.; Swaim, S. F.; Lauten, S. D.; Garner, C. A.; Boudreaux, M. K.; Spano, J. S.; Hoffman, C. E.; Conner, B., 1994: Evaluation of effects of dietary n-6 to n-3 fatty acid ratios on leukotriene B synthesis in dog skin and neutrophils. Veterinary Dermatology 5, 163-173.
81. Wander, R. C.; Hall, J. A.; Gradin, J. L.; Du, S. H.; Jewell, D. E., 1997: The ratio of dietary (n-6) to (n-3) fatty acids influences immune system function, eicosanoid metabolism, lipid peroxidation and vitamin E status in aged dogs. Journal of Nutrition 127, 1198-1205.
82. Wang, Y.; Oram, J. F., 2005: Unsaturated fatty acids phosphorylate and destabilize ABCA1 through a phospholipase D2 pathway. Journal of Biological Chemistry 280, 35896-35903.
83. Wassall, S. R.; Stillwell, W., 2008: Docosahexaenoic acid domains: the ultimate non-raft membrane domain. Chemistry and Physics of Lipids 153, 57-63.
84. Yaqoob, P., 2010: Mechanisms underlying the immunomodulatory effects of n-3 PUFA. Proceedings of the Nutrition Society 69, 311-315.
85. Yi, L.; Zhang, Q. Y.; Mi, M. T., 2007: Role of Rho GTPase in inhibiting metastatic ability of human prostate cancer cell line PC-3 by omega-3 polyunsaturated fatty acid. Ai Zheng 26, 1281-1286.
86. Young, C.; Gean, P. W.; Chiou, L. C.; Shen, Y. Z., 2000: Docosahexaenoic acid inhibits synaptic transmission and epileptiform activity in the rat hippocampus. Synapse (New York, N. Y.) 37, 90-94.