Regulation of physiological and pathological Th1 and Th2 responses by lactoferrin

Biochemistry and Cell Biology

Volumn 84, Issue 3, 2006, Pages 303-311

  Fischer, Romy ^a,b   Debbabi, Hajer ^a   Dubarry, Michel ^a   Boyaka, Prosper ^b   Tomé, Daniel ^a  

^a INRA Institut National de la Recherche Agronomique   (France)

^b University of Alabama at Birmingham   (United States)

Author keywords

Immunoregulatory properties; Lactoferrin; Th responses

Indexed keywords

CELLS; DISEASES; IMMUNOLOGY; MICROBIOLOGY; MICROORGANISMS; PATHOLOGY; PHYSIOLOGY; TUMORS;

IMMUNOREGULATORY PROPERTIES; LACTOFERRIN; TH RESPONSES;

PROTEINS;

LACTOFERRIN;

ALLERGIC DISEASE; AUTOIMMUNE DISEASE; CELL ACTIVITY; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CONFERENCE PAPER; DRUG MECHANISM; HUMAN; IMMUNE STATUS; IMMUNOREGULATION; INFLAMMATION; NONHUMAN; PATHOPHYSIOLOGY; TH1 CELL; TH2 CELL; THYMOCYTE;

ADMINISTRATION, ORAL; ANIMALS; ANTIBODIES; CELL DIFFERENTIATION; CELL PROLIFERATION; COMMUNICABLE DISEASES; CYTOKINES; INFLAMMATION; LACTOFERRIN; MICE; MICE, INBRED C57BL; MODELS, BIOLOGICAL; TH1 CELLS; TH2 CELLS; TOXOPLASMA;

MAMMALIA;

EID: 33748418332     PISSN: 08298211     EISSN: None     Source Type: Journal    
DOI: 10.1139/O06-058     Document Type: Conference Paper

References (80)

1. Abbas, A.K., Murphy, K.M., and Sher, A. 1996. Functional diversity of helper T lymphocytes. Nature (London), 383: 787-793. doi:10.1038/383787a0. PMID: 8893001.
2. Appelmelk, B.J., An, Y.Q., Geerts, M., Thijs, B.G., de Boer, H.A., MacLaren, D.M., de Graaff, J., and Nuijens, J.H. 1994. Lactoferrin is a lipid A-binding protein. Infect. Immun. 62: 2628-2632. PMID: 8188389.
3. Ashorn, R.G., Eskola, J., Tuohimaa, P.J., and Krohn, K.J. 1986. Effect of the progesterone-inducible proteins human lactoferrin and chicken avidin on lymphocyte proliferation. Hum. Reprod. 1: 149-151. PMID: 2957386.
4. Beutler, B., and Cerami, A. 1987. The endogenous mediator of endotoxic shock. Clin. Res. 35: 192-197. PMID: 3552383.
5. Bezault, J., Bhimani, R., Wiprovnick, J., and Furmanski, P. 1994. Human lactoferrin inhibits growth of solid tumors and development of experimental metastases in mice. Cancer Res. 54: 2310-2312. PMID: 8162571.
6. Bhimani, R.S., Vendrov, Y., and Furmanski, P. 1999. Influence of lactoferrin feeding and injection against systemic staphylococcal infections in mice. J. Appl. Microbiol. 86: 135-144. doi:10.1046/j.1365-2672.1999.00644.x. PMID: 10030017.
7. Bi, B.Y., Lefebvre, A.M., Dus, D., Spik, G., and Mazurier, J. 1997. Effect of lactoferrin on proliferation and differentiation of the Jurkat human lymphoblastic T cell line. Arch. Immunol. Ther. Exp. (Warsz.), 45: 315-320. PMID: 9523007.
8. Birgens, H.S. 1994. The monocytic receptor for lactoferrin and its involvement in lactoferrin-mediated iron transport. Adv. Exp. Med. Biol. 357: 99-109. PMID: 7762450.
9. Buderus, S., Boone, J., Lyerly, D., and Lentze, M.J. 2004. Fecal lactoferrin: a new parameter to monitor infliximab therapy. Dig. Dis. Sci. 49: 1036-1039. doi:10.1023/B:DDAS.0000034568.69407.47. PMID: 15309897.
10. Caccavo, D., Sebastiani, G.D., Di Monaco, C., Guido, F., Galeazzi, M., Ferri, G.M., Bonomo, L., and Afeltra, A. 1999. Increased levels of lactoferrin in synovial fluid but not in serum from patients with rheumatoid arthritis. Int. J. Clin. Lab. Res. 29: 30-35. doi:10.1007/s005990050059. PMID: 10356661.
11. Crouch, S.P., Slater, K.J., and Fletcher, J. 1992. Regulation of cytokine release from mononuclear cells by the iron-binding protein lactoferrin. Blood, 80: 235-240. PMID: 1535239.
12. Cumberbatch, M., Dearman, R.J., Uribe-Luna, S., Headon, D.R., Ward, P.P., Conneely, O.M., and Kimber, I. 2000. Regulation of epidermal Langerhans cell migration by lactoferrin. Immunology, 100: 21-28. doi:10.1046/j.1365-2567.2000. 00014.x. PMID: 10809955.
13. Cumberbatch, M., Dearman, R.J., Griffiths, C.E., and Kimber, I. 2003. Epidermal Langerhans cell migration and sensitization to chemical allergens. APMIS, 111: 797-804. doi:10.1034/j.1600-0463.2003.11107811.x. PMID: 12974781.
14. Debbabi, H. 1997. Absorption and immunomodulatory effects of bovine lactoferrin in mice. Ph.D. thesis. INA P-G, Paris, France.
15. Debbabi, H., Dubarry, M., Rautureau, M., and Tome, D. 1998. Bovine lactoferrin induces both mucosal and systemic immune response in mice. J. Dairy Res. 65: 283-293. doi:10.1017/S0022029997002732. PMID: 9627847.
16. Dhennin-Duthille, I., Masson, M., Damiens, E., Fillebeen, C., Spik, G., and Mazurier, J. 2000. Lactoferrin upregulates the expression of CD4 antigen through the stimulation of the mitogen-activated protein kinase in the human lymphoblastic T Jurkat cell line. J. Cell. Biochem. 79: 583-593. doi:10.1002/1097-4644(20001215)79:4<583::AID-JCB70>3.0.CO;2-9. PMID: 10996849.
17. Dwarakanath, A.D., Finnie, I.A., Beesley, C.M., O'Dowd, G.M., Nash, J., Tsai, H.H., Parker, N., and Rhodes, J.M. 1997. Differential excretion of leucocyte granule components in inflammatory bowel disease: implications for pathogenesis. Clin. Sci. (London), 92: 307-313. PMID: 9093012.
18. Elass-Rochard, E., Roseanu, A., Legrand, D., Trif, M., Salmon, V., Motas, C., Montreuil, J., and Spik, G. 1995. Lactoferrin-lipopolysaccharide interaction: involvement of the 28-34 loop region of human lactoferrin in the high-affinity binding to Escherichia coli 055B5 lipopolysaccharide. Biochem. J. 312: 839-845. PMID: 8554529.
19. Elass-Rochard, E., Legrand, D., Salmon, V., Roseanu, A., Trif, M., Tobias, P.S., Mazurier, J., and Spik, G. 1998. Lactoferrin inhibits the endotoxin interaction with CD14 by competition with the lipopolysaccharide- binding protein. Infect. Immun. 66: 486-491. PMID: 9453600.
20. Elrod, K.C., Moore, W.R., Abraham, W.M., and Tanaka, R.D. 1997. Lactoferrin, a potent tryptase inhibitor, abolishes late-phase airway responses in allergic sheep. Am. J. Respir. Crit. Care Med. 156: 375-381. PMID: 9279212.
21. Griffiths, C.E., Cumberbatch, M., Tucker, S.C., Dearman, R.J., Andrew, S., Headon, D.R., and Kimber, I. 2001. Exogenous topical lactoferrin inhibits allergen-induced Langerhans cell migration and cutaneous inflammation in humans. Br. J. Dermatol. 144: 715-725. doi:10.1046/j.1365-2133.2001.04125.x. PMID: 11298528.
22. Guillen, C., McInnes, I.B., Vaughan, D., Speekenbrink, A.B., and Brock, J.H. 2000. The effects of local administration of lactoferrin on inflammation in murine autoimmune and infectious arthritis. Arthritis Rheum. 43: 2073-2080. doi:10.1002/1529-0131(200009)43:9<2073::AID-ANR19>3.0.CO;2-U. PMID: 11014359.
23. Guillen, C., McInnes, I.B., Vaughan, D.M., Kommajosyula, S., Van Berkel, P.H., Leung, B.P., Aguila, A., and Brock, J.H. 2002. Enhanced Th1 response to Staphylococcus aureus infection in human lactoferrin-transgenic mice. J. Immunol. 168: 3950-3957. PMID: 11937551.
24. Gutteberg, T.J., Rokke, O., Andersen, O., and Jorgensen, T. 1989. Early fall of circulating iron and rapid rise of lactoferrin in septicemia and endotoxemia: an early defence mechanism. Scand. J. Infect. Dis. 21: 709-715. PMID: 2694351.
25. Haversen, L.A., Engberg, I., Baltzer, L., Dolphin, G., Hanson, L.A., and Mattsby-Baltzer, I. 2000. Human lactoferrin and peptides derived from a surface-exposed helical region reduce experimental Escherichia coli urinary tract infection in mice. Infect. Immun. 68: 5816-5823. doi:10.1128/IAI.68.10. 5816-5823.2000. PMID: 10992490.
26. Haversen, L., Ohlsson, B.G., Hahn-Zoric, M., Hanson, L.A., and Mattsby-Baltzer, I. 2002. Lactoferrin down-regulates the LPS-induced cytokine production in monocytic cells via NF-kappa B. Cell. Immunol. 220: 83-95. PMID: 12657243.
27. Haversen, L.A., Baltzer, L., Dolphin, G., Hanson, L.A., and Mattsby-Baltzer, I. 2003. Anti-inflammatory activities of human lactoferrin in acute dextran sulphate-induced colitis in mice. Scand. J. Immunol. 57: 2-10. doi:10.1046/j.1365-3083.2003.01162.x. PMID: 12542792.
28. He, S., McEuen, A.R., Blewett, S.A., Li, P., Buckley, M.G., Leufkens, P., and Walls, A.F. 2003. The inhibition of mast cell activation by neutrophil lactoferrin: uptake by mast cells and interaction with tryptase, chymase and cathepsin G. Biochem. Pharmacol. 65: 1007-1015. doi:10.1016/S0006-2952(02)01651- 9. PMID: 12623133.
29. Iigo, M., Kuhara, T., Ushida, Y., Sekine, K., Moore, M.A., and Tsuda, H. 1999. Inhibitory effects of bovine lactoferrin on colon carcinoma 26 lung metastasis in mice. Clin. Exp. Metastasis, 17: 35-40. PMID: 10390145.
30. Ishii, K., Takamura, N., Shinohara, M., Wakui, N., Shin, H., Sumino, Y., et al. 2003. Long-term follow-up of chronic hepatitis C patients treated with oral lactoferrin for 12 months. Hepatol. Res. 25: 226-233. PMID: 12697243.
31. Iwasa, M., Kaito, M., Ikoma, J., Takeo, M., Imoto, I., Adachi, Y., et al. 2002. Lactoferrin inhibits hepatitis C virus viremia in chronic hepatitis C patients with high viral loads and HCV genotype 1b. Am. J. Gastroenterol. 97: 766-767. doi:10.1111/j.1572-0241.2002.05573.x. PMID: 11922584.
32. Kane, S.V., Sandborn, W.J., Rufo, P.A., Zholudev, A., Boone, J., Lyerly, D., Camilleri, M., and Hanauer, S.B. 2003. Fecal lactoferrin is a sensitive and specific marker in identifying intestinal inflammation. Am. J. Gastroenterol. 98: 1309-1314. doi:10.1111/j.1572-0241.2003.07458.x. PMID: 12818275.
33. Kimber, I., Cumberbatch, M., Dearman, R.J., Headon, D.R., Bhushan, M., and Griffiths, C.E. 2002. Lactoferrin: influences on Langerhans cells, epidermal cytokines, and cutaneous inflammation. Biochem. Cell Biol. 80: 103-107. doi:10.1139/o01-227. PMID: 11911118.
34. Kruzel, M.L., Harari, Y., Chen, C.Y., and Castro, G.A. 2000. Lactoferrin protects gut mucosal integrity during endotoxemia induced by lipopolysaccharide in mice. Inflammation, 24: 33-44. doi:10.1023/A:1006935908960. PMID: 10704062.
35. Kruzel, M.L., Harari, Y., Mailman, D., Actor, J.K., and Zimecki, M. 2002. Differential effects of prophylactic, concurrent and therapeutic lactoferrin treatment on LPS-induced inflammatory responses in mice. Clin. Exp. Immunol. 130: 25-31. doi:10.1046/j.1365-2249.2002.01956.x. PMID: 12296849.
36. Kuhara, T., Iigo, M., Itoh, T., Ushida, Y., Sekine, K., Terada, N., Okamura, H., and Tsuda, H. 2000. Orally administered lactoferrin exerts an antimetastatic effect and enhances production of IL-18 in the intestinal epithelium. Nutr. Cancer, 38: 192-199. PMID: 11525597.
37. Levay, P.F., and Viljoen, M. 1995. Lactoferrin: a general review. Haematologica, 80: 252-267. PMID: 7672721.
38. Lima, M.F., and Kierszenbaum, F. 1985. Lactoferrin effects on phagocytic cell function. I. Increased uptake and killing of an intracellular parasite by murine macrophages and human monocytes. J. Immunol. 134: 4176-4183. PMID: 3886800.
39. Mauri, C., Williams, R.O., Walmsley, M., and Feldmann, M. 1996. Relationship between Th1/Th2 cytokine patterns and the arthritogenic response in collagen-induced arthritis. Eur. J. Immunol. 26: 1511-1518. PMID: 8766554.
40. Moed, H., Boorsma, D.M., Stoof, T.J., von Blomberg, B.M., Bruynzeel, D.P., Scheper, R.J., Gibbs, S., and Rustemeyer, T. 2004. Nickel-responding T cells are CD4+ CLA+ CD45RO+ and express chemokine receptors CXCR3, CCR4 and CCR10. Br. J. Dermatol. 151: 32-41. doi:10.1111/j.1365-2133.2004.05975.x. PMID: 15270870.
41. Mosmann, T.R., Cherwinski, H., Bond, M.W., Giedlin, M.A., and Coffman, R.L. 1986. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J. Immunol. 136: 2348-2357. PMID: 2419430.
42. Murphy, M.E., Kariwa, H., Mizutani, T., Tanabe, H., Yoshimatsu, K., Arikawa, J., and Takashima, I. 2001. Characterization of in vitro and in vivo antiviral activity of lactoferrin and ribavirin upon hantavirus. J. Vet. Med. Sci. 63: 637-645. doi:10.1292/jvms.63.637. PMID: 11459009.
43. Paul, W.E., and Seder, R.A. 1994. Lymphocyte responses and cytokines. Cell, 76: 241-251. doi:10.1016/0092-8674(94)90332-8. PMID: 7904900.
44. Penco, S., Pastorino, S., Bianchi-Scarra, G., and Garre, C. 1995. Lactoferrin down-modulates the activity of the granulocyte macrophage colony-stimulating factor promoter in interleukin-1 beta-stimulated cells. J. Biol. Chem. 270: 12263-12268. PMID: 7744878.
45. Richie, E.R., Hilliard, J.K., Gilmore, R., and Gillespie, D.J. 1987. Human milk-derived lactoferrin inhibits mitogen and alloantigen induced human lymphocyte proliferation. J. Reprod. Immunol. 12: 137-148. PMID: 2963123.
46. Romagnani, S. 1994. Lymphokine production by human T cells in disease states. Annu. Rev. Immunol. 12: 227-257. doi:10.1146/annurev.iy.12.040194. 001303. PMID: 8011282.
47. Romagnani, S. 2000. The role of lymphocytes in allergic disease. J. Allergy Clin. Immunol. 105: 399-408. doi:10.1067/mai.2000.104575. PMID: 10719286.
48. Sfeir, R.M., Dubarry, M., Boyaka, P.N., Rautureau, M., and Tome, D. 2004. The mode of oral bovine lactoferrin administration influences mucosal and systemic immune responses in mice. J. Nutr. 134: 403-409. PMID: 14747680.
49. Slater, K., and Fletcher, J. 1987. Lactoferrin derived from neutrophils inhibits the mixed lymphocyte reaction. Blood, 69: 1328-1333. PMID: 2952183.
50. Smith, S.R., Calzetta, A., Bankowski, J., Kenworthy-Bott, L., and Terminelli, C. 1993. Lipopolysaccharide-induced cytokine production and mortality in mice treated with Corynebacterium parvum. J. Leukoc. Biol. 54: 23-29. PMID: 8336076.
51. Sugi, K., Saitoh, O., Hirata, I., and Katsu, K. 1996. Fecal lactoferrin as a marker for disease activity in inflammatory bowel disease: comparison with other neutrophil-derived proteins. Am. J. Gastroenterol. 91: 927-934. PMID: 8633583.
52. Takakura, N., Wakabayashi, H., Ishibashi, H., Teraguchi, S., Tamura, Y., Yamaguchi, H., and Abe, S. 2003. Oral lactoferrin treatment of experimental oral candidiasis in mice. Antimicrob. Agents Chemother. 47: 2619-2623. doi:10.1128/AAC.47.8.2619-2623.2003. PMID: 12878528.
53. Takakura, N., Wakabayashi, H., Ishibashi, H., Yamauchi, K., Teraguchi, S., Tamura, Y., Yamaguchi, H., and Abe, S. 2004. Effect of orally administered bovine lactoferrin on the immune response in the oral candidiasis murine model. J. Med. Microbiol. 53: 495-500. PMID: 15150327.
54. Tanaka, K., Ikeda, M., Nozaki, A., Kato, N., Tsuda, H., Saito, S., and Sekihara, H. 1999. Lactoferrin inhibits hepatitis C virus viremia in patients with chronic hepatitis C: a pilot study. Jpn. J. Cancer Res. 90: 367-371. PMID: 10363572.
55. Tanaka, T., Abe, Y., Inoue, N., Kim, W.S., Kumura, H., Nagasawa, H., Igarashi, I., and Shimazaki, K. 2004. The detection of bovine lactoferrin binding protein on Trypanosoma brucei. J. Vet. Med. Sci. 66: 619-625. doi:10.1292/jvms.66.619. PMID: 15240935.
56. Teraguchi, S., Shin, K., Ogata, T., Kingaku, M., Kaino, A., Miyauchi, H., Fukuwatari, Y., and Shimamura, S. 1995. Orally administered bovine lactoferrin inhibits bacterial translocation in mice fed bovine milk. Appl. Environ. Microbiol. 61: 4131-4134. PMID: 8526530.
57. Thompson, A.B., Bohling, T., Payvandi, F., and Rennard, S.I. 1990. Lower respiratory tract lactoferrin and lysozyme arise primarily in the airways and are elevated in association with chronic bronchitis. J. Lab. Clin. Med. 115: 148-158. PMID: 2299262.
58. Togawa, J., Nagase, H., Tanaka, K., Inamori, M., Nakajima, A., Ueno, N., Saito, T., and Sekihara, H. 2002a. Oral administration of lactoferrin reduces colitis in rats via modulation of the immune system and correction of cytokine imbalance. J. Gastroenterol. Hepatol. 17: 1291-1298. doi:10.1046/j.1440-1746. 2002.02868.x. PMID: 12423274.
59. Togawa, J., Nagase, H., Tanaka, K., Inamori, M., Umezawa, T., Nakajima, A., et al. 2002b. Lactoferrin reduces colitis in rats via modulation of the immune system and correction of cytokine imbalance. Am. J. Physiol. Gastrointest. Liver Physiol. 283: G187-G195. PMID: 12065306.
60. Tsokos, M., and Paulsen, F. 2002. Expression of pulmonary lactoferrin in sudden-onset and slow-onset asthma with fatal outcome. Virchows Arch. 441: 494-499. PMID: 12447681.
61. Uchida, K., Matsuse, R., Tomita, S., Sugi, K., Saitoh, O., and Ohshiba, S. 1994. Immunochemical detection of human lactoferrin in feces as a new marker for inflammatory gastrointestinal disorders and colon cancer. Clin. Biochem. 27: 259-264. PMID: 8001286.
62. van de Graaf, E.A., Out, T.A., Kobesen, A., and Jansen, H.M. 1991. Lactoferrin and secretory IgA in the bronchoalveolar lavage fluid from patients with a stable asthma. Lung, 169: 275-283. PMID: 1745058.
63. Wada, T., Aiba, Y., Shimizu, K., Takagi, A., Miwa, T., and Koga, Y. 1999. The therapeutic effect of bovine lactoferrin in the host infected with Helicobacter pylori. Scand. J. Gastroenterol. 34: 238-243. PMID: 10232866.
64. Wakabayashi, H., Uchida, K., Yamauchi, K., Teraguchi, S., Hayasawa, H., and Yamaguchi, H. 2000. Lactoferrin given in food facilitates dermatophytosis cure in guinea pig models. J. Antimicrob. Chemother. 46: 595-602. doi:10.1093/jac/46.4.595. PMID: 11020258.
65. Wakabayashi, H., Takakura, N., Yamauchi, K., Teraguchi, S., Uchida, K., Yamaguchi, H., and Tamura, Y. 2002. Effect of lactoferrin feeding on the host antifungal response in guinea-pigs infected or immunised with Trichophyton mentagrophytes. J. Med. Microbiol. 51: 844-850. PMID: 12435063.
66. Wakabayashi, H., Takakura, N., Teraguchi, S., and Tamura, Y. 2003. Lactoferrin feeding augments peritoneal macrophage activities in mice intraperitoneally injected with inactivated Candida albicans. Microbiol. Immunol. 47: 37-43. PMID: 12636251.
67. Wakabayashi, H., Kurokawa, M., Shin, K., Teraguchi, S., Tamura, Y., and Shiraki, K. 2004. Oral lactoferrin prevents body weight loss and increases cytokine responses during herpes simplex virus type 1 infection of mice. Biosci. Biotechnol. Biochem. 68: 537-544. doi:10.1271/bbb.68.537. PMID: 15056884.
68. Wang, W.P., Iigo, M., Sato, J., Sekine, K., Adachi, I., and Tsuda, H. 2000. Activation of intestinal mucosal immunity in tumor-bearing mice by lactoferrin. Jpn. J. Cancer Res. 91: 1022-1027. PMID: 11050473.
69. Ward, P.P., Paz, E., and Conneely, O.M. 2005. Multifunctional roles of lactoferrin: a critical overview. Cell. Mol. Life Sci. 62: 2540-2548. doi:10.1007/s00018-005-5369-8. PMID: 16261256.
70. Wong, C.W., Seow, H.F., Husband, A.J., Regester, G.O., and Watson, D.L. 1997. Effects of purified bovine whey factors on cellular immune functions in ruminants. Vet. Immunol. Immunopathol. 56: 85-96. PMID: 9220583.
71. Yamauchi, K., Tomita, M., Giehl, T.J., and Ellison, R.T., III. 1993. Antibacterial activity of lactoferrin and a pepsin-derived lactoferrin peptide fragment. Infect. Immun. 61: 719-728. PMID: 8423097.
72. Yamauchi, K., Hiruma, M., Yamazaki, N., Wakabayashi, H., Kuwata, H., Teraguchi, S., et al. 2000. Oral administration of bovine lactoferrin for treatment of tinea pedis. A placebo-controlled, double-blind study. Mycoses, 43: 197-202. doi:10.1046/j.1439-0507.2000.00571.x. PMID: 10948819.
73. Zagulski, T., Lipinski, P., Zagulska, A., Broniek, S., and Jarzabek, Z. 1989. Lactoferrin can protect mice against a lethal dose of Escherichia coli in experimental infection in vivo. Br. J. Exp. Pathol. 70: 697-704. PMID: 2690922.
74. Zagulski, T., Lipinski, P., Zagulska, A., and Jarzabek, Z. 1998. Antibacterial system generated by lactoferrin in mice in vivo is primarily a killing system. Int. J. Exp. Pathol. 79: 117-123. PMID: 9709381.
75. Zimecki, M., Mazurier, J., Machnicki, M., Wieczorek, Z., Montreuil, J., and Spik, G. 1991. Immunostimulatory activity of lactotransferrin and maturation of CD4- CD8- murine thymocytes. Immunol. Lett. 30: 119-123. doi:10.1016/0165-2478(91)90099-V. PMID: 1683650.
76. Zimecki, M., Mazurier, J., Spik, G., and Kapp, J.A. 1996. Lactoferrin inhibits proliferative response and cytokine production of TH1 but not TH2 cell lines. Arch. Immunol. Ther. Exp. (Warsz.), 44: 51-56. PMID: 8874770.
77. Zimecki, M., Miedzybrodzki, R., and Szymaniec, S. 1998. Oral treatment of rats with bovine lactoferrin inhibits carrageenan-induced inflammation; correlation with decreased cytokine production. Arch. Immunol. Ther. Exp. (Warsz.), 46: 361-365. PMID: 9883315.
78. Zimecki, M., Stepniak, D., Szynol, A., and Kruzel, M.L. 2001. Lactoferrin regulates proliferative response of human peripheral blood mononuclear cells to phytohemagglutinin and mixed lymphocyte reaction. Arch. Immunol. Ther. Exp. (Warsz.), 49: 147-154. PMID: 11348019.
79. Zimecki, M., Chodaczek, G., Kocieba, M., and Kruzel, M.L. 2004. Lethality in LPS-induced endotoxemia in C3H/HeCr mice is associated with prevalence of proinflammatory cytokines: lack of protective action of lactoferrin. FEMS Immunol. Med. Microbiol. 42: 167-172. doi:10.1016/j.femsim.2004.04.003. PMID: 15364100.
80. Zweiman, B., Kucich, U., Shalit, M., Von Allmen, C., Moskovitz, A., Weinbaum, G., and Atkins, P.C. 1990. Release of lactoferrin and elastase in human allergic skin reactions. J. Immunol. 144: 3953-3960. PMID: 1692068.