Bovine lactoferrin inhibits lung cancer growth through suppression of both inflammation and expression of vascular endothelial growth factor

Journal of Dairy Science

Volumn 96, Issue 4, 2013, Pages 2095-2106

  Tung, Yu Tang ^a   Chen, Hsiao Ling ^b   Yen, Chih Ching ^a,c   Lee, Po Ying ^d   Tsai, Hsin Chung ^a,e   Lin, Ming Fong ^a,e   Chen, Chuan Mu ^a  

^a NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^b DA YEH UNIVERSITY   (Taiwan)

^c CHINA MEDICAL UNIVERSITY   (Taiwan)

^d NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^e TAICHUNG HOSPITAL   (Taiwan)

Author keywords

Bovine lactoferrin; Pulmonary cancer; Transgenic mice; Vascular endothelial growth factor (VEGF)

Indexed keywords

ANGIOGENESIS INHIBITOR; ANTIINFLAMMATORY AGENT; ANTINEOPLASTIC AGENT; CYTOKINE; INTERLEUKIN 6; LACTOFERRIN; MESSENGER RNA; PEPTIDE FRAGMENT; TUMOR NECROSIS FACTOR ALPHA; VASCULAR ENDOTHELIAL GROWTH FACTOR A (138 165); VASCULAR ENDOTHELIAL GROWTH FACTOR A (138-165); VASCULOTROPIN A;

ANIMAL; ARTICLE; CATTLE; CELL PROLIFERATION; DRUG ANTAGONISM; DRUG EFFECT; GENE EXPRESSION; GENETICS; HUMAN; LUNG TUMOR; MOUSE; PATHOLOGY; TRANSGENIC MOUSE; TUMOR CELL LINE;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTI-INFLAMMATORY AGENTS; ANTINEOPLASTIC AGENTS; CATTLE; CELL LINE, TUMOR; CELL PROLIFERATION; CYTOKINES; GENE EXPRESSION; HUMANS; INTERLEUKIN-6; LACTOFERRIN; LUNG NEOPLASMS; MICE; MICE, TRANSGENIC; PEPTIDE FRAGMENTS; RNA, MESSENGER; TUMOR NECROSIS FACTOR-ALPHA; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

BOVINAE; MUS MUSCULUS;

EID: 84875550832     PISSN: 00220302     EISSN: 15253198     Source Type: Journal    
DOI: 10.3168/jds.2012-6153     Document Type: Article

References (41)

1. Alas S., Emmanouilides C., Bonavida B. Inhibition of interleukin 10 by rituximab results in down-regulation of bcl-2 and sensitization of B-cell non-Hodgkin's lymphoma to apoptosis. Clin. Cancer Res 2001, 7:709-723.
2. Bohlen H., Kessler M., Sextro M., Diehl V., Tesch H. Poor clinical outcome of patients with Hodgkin's disease and elevated interleukin-10 serum levels. Clinical significance of interleukin-10 serum levels for Hodgkin's disease. Ann. Hematol. 2000, 79:110-113.
3. Chang C.C., Shih J.Y., Jeng Y.M., Su J.L., Lin B.Z., Chen S.T., Chau Y.P., Yang P.C., Kuo M.L. Connective tissue growth factor and its role in lung adenocarcinoma invasion and metastasis. J. Natl. Cancer Inst 2004, 96:364-375.
4. Chen C.M., Chen H.L., Hsiau T.H.C., Hsiau A.H., Shi H., Brock G.J., Wei S.H., Caldwell C.W., Yan P.S., Huang T.H. Methylation target array for rapid analysis of CpG island hypermethylation in multiple tissue genomes. Am. J. Pathol. 2003, 163:37-45.
5. Chen H.L., Huang J.Y., Chu T.W., Tsai T.C., Hung C.M., Lin C.C., Liu F.C., Wang L.C., Chen Y.J., Lin M.F., Chen C.M. Expression of VP1 protein in the milk of transgenic mice: A potential oral vaccine against enterovirus 71 infection. Vaccine 2008, 26:2882-2889.
6. Chen H.L., Lai Y.W., Chen C.S., Chu T.W., Lin W., Yen C.C., Lin M.F., Tu M.Y., Chen C.M. Probiotic Lactobacillus casei expressing human lactoferrin elevates antibacterial activity in the gastrointestinal tract. Biometals 2010, 23:543-554.
7. Chen H.L., Wang L.C., Chang C.H., Yen C.C., Cheng W.T., Wu S.C., Hung C.M., Kuo M.F., Chen C.M. Recombinant porcine lactoferrin expressed in the milk of transgenic mice protects neonatal mice from a lethal challenge with enterovirus type 71. Vaccine 2008, 26:891-898.
8. Chen J.J., Peck K., Hong T.M., Yang S.C., Sher Y.P., Shih J.Y., Wu R., Cheng J.L., Roffler S.R., Wu C.W., Yang P.C. Global analysis of gene expression in invasion by a lung cancer model. Cancer Res 2001, 61:5223-5230.
9. Chen Y.J., Wu C.Y., Chang C.C., Ma C.J., Li M.C., Chen C.M. Nuclear Kruppel-like factor 4 expression is associated with human skin squamous cell carcinoma progression and metastasis. Cancer Biol. Ther. 2008, 7:777-782.
10. Chen Y.J., Wu C.Y., Shen J.L., Chu S.Y., Chen C.K., Chang Y.T., Chen C.M. Psoriasis independently associated with hyperleptinemia contributing to metabolic syndrome. Arch. Dermatol. 2008, 144:1571-1575.
11. Coussens L.M., Werb Z. Inflammation and cancer. Nature 2002, 420:860-867.
12. de Mejia E.G., Dia V.P. The role of nutraceutical proteins and peptides in apoptosis, angiogenesis, and metastasis of cancer cells. Cancer Metastasis Rev 2010, 29:511-528.
13. Duarte D.C., Nicolau A., Teixeira J.A., Rodrigues L.R. The effect of bovine milk lactoferrin on human breast cancer cell lines. J. Dairy Sci 2011, 94:66-76.
14. Ferlay J., Shin H.R., Bray F., Forman D., Mathers C., Parkin D.M. Estimates of worldwide burden of cancer in 2008. Int. J. Cancer. 2010, 127:2893-2917.
15. Ferrara N. VEGF and the request for tumor angiogenesis factors. Nat. Rev. Cancer. 2002, 2:795-803.
16. Ferrara N., Davis-Smyth T. The biology of vascular endothelial growth factor. Endocr. Rev. 1997, 18:4-25.
17. González-Chávez S.A., Arévalo-Gallegos S., Rascón-Cruz Q. Lactoferrin: Structure, function and applications. Int. J. Antimicrob. Agents. 2009, 33:301-306.
18. Hong D.S., Angelo L.S., Kurzrock R. Interleukin-6 and its receptor in cancer: implications for translational therapeutics. Cancer 2007, 110:1911-1928.
19. Hung C.M., Yeh C.C., Chen H.L., Lai C.W., Kuo M.F., Yeh M.H., Lin W., Tu M.Y., Cheng H.C., Chen C.M. Porcine lactoferrin administration enhances peripheral lymphocyte proliferation and assists infectious bursal disease vaccination in native chickens. Vaccine 2010, 28:2895-2902.
20. Li A.F., Hsu H.S., Hsu C.Y., Li A.C., Li W.Y., Liang W.Y., Chen J.Y. A 20-year retrospective study of small-cell carcinomas in Taiwan. J. Surg. Oncol. 2010, 102:497-502.
21. Li D., Sakashita S., Morishita Y., Kano J., Shiba A., Sato T., Noguchi M. Binding of lactoferrin to IGBP1 triggers apoptosis in a lung adenocarcinoma cell line. Anticancer Res 2011, 31:529-534.
22. Lin S.S., Lai K.C., Hsu S.C., Yang J.S., Kuo C.L., Lin J.P., Ma Y.S., Wu C.C., Chung J.G. Curcumin inhibits the migration and invasion of human A549 lung cancer cells through the inhibition of matrix metalloproteinase-2 and -9 and vascular endothelial growth factor (VEGF). Cancer Lett 2009, 285:127-133.
23. Liu F.C., Chen H.L., Chong K.Y., Hsu A.L., Chen C.M. Production of recombinant porcine colipase secreted by Pichia pastoris and its application to improve dietary fat digestion and growth of postweaning piglets. Biotechnol. Prog. 2008, 24:1333-1341.
24. Lönnerdal B., Iyer S. Lactoferrin: Molecular structure and biological function. Annu. Rev. Nutr. 1995, 15:93-110.
25. Masuda C., Wanibuchi H., Sekine K., Yano Y., Otani S., Kishimoto T., Tsuda H., Fukushima S. Chemopreventive effects of bovine lactoferrin on N-butyl-N-(4-hydroxybutyl) nitrosamine-induced rat bladder carcinogenesis. Jpn. J. Cancer Res 2000, 91:582-588.
26. Rodrigues L., Teixeira J., Schmitt F., Paulsson M., Månsson H.L. Lactoferrin and cancer disease prevention. Crit. Rev. Food Sci. Nutr. 2009, 49:203-217.
27. Sethi G., Sung B., Aggarwal B.B. TNF: A master switch for inflammation to cancer. Front. Biosci. 2008, 13:5094-5107.
28. Shimamura M., Yamamoto Y., Ashino H., Oikawa T., Hazato T., Tsuda H., Iigo M. Bovine lactoferrin inhibits tumor-induced angiogenesis. Int. J. Cancer. 2004, 111:111-116.
29. Singh A.V., Franke A.A., Blackburn G.L., Zhou J.R. Soy phytochemicals prevent orthotopic growth and metastasis of bladder cancer in mice by alterations of cancer cell proliferation and apoptosis and tumor angiogenesis. Cancer Res 2006, 66:1851-1858.
30. Sredni B., Weil M., Khomenok G., Lebenthal I., Teitz S., Mardor Y., Ram Z., Orenstein A., Kershenovich A., Michowiz S., Cohen Y.I., Rappaport Z.H., Freidkin I., Albeck M., Longo D.L., Kalechman Y. Ammonium trichloro(dioxoethylene-o,o')tellurate (AS101) sensitizes tumors to chemotherapy by inhibiting the tumor interleukin 10 autocrine loop. Cancer Res 2004, 64:1843-1852.
31. Tanaka T., Kawabata K., Kohno H., Honjo S., Murakami M., Ota T., Tsuda H. Chemopreventive effect of bovine lactoferrin on 4-nitroquinoline 1-oxide-induced tongue carcinogenesis in male F344 rats. Jpn. J. Cancer Res 2000, 91:25-33.
32. Tsai T.C., Lin W., Yang S.H., Cheng W.T., Cheng E.H., Lee M.S., Chong K.Y., Chen C.M. Granzyme G is expressed in the two-cell stage mouse embryo and is required for the maternal-zygotic transition. BMC Dev. Biol. 2010, 10:88.
33. Tsuda H., Sekine K., Nakamura J., Ushida Y., Kuhara T., Takasuka N., Kim D.J., Asamoto M., Baba-Toriyama H., Moore M.A., Nishino H., Kakizoe T. Inhibition of azoxymethane initiated colon tumor and aberrant crypt foci development by bovine lactoferrin administration in F344 rats. Adv. Exp. Med. Biol. 1998, 443:273-284.
34. Tung Y.T., Chen H.L., Lai C.W., Shen C.J., Lai Y.W., Chen C.M. Curcumin reduces pulmonary tumorigenesis in vascular endothelial growth factor (VEGF)-overexpressing transgenic mice. Mol. Nutr. Food Res 2011, 55:1036-1043.
35. Ushida Y., Sekine K., Kuhara T., Takasuka N., Iigo M., Maeda M., Tsuda H. Possible chemopreventive effects of bovine lactoferrin on esophagus and lung carcinogenesis in the rat. Jpn. J. Cancer Res 1999, 90:262-267.
36. Xu X.X., Jiang H.R., Li H.B., Zhang T.N., Zhou Q., Liu N. Apoptosis of stomach cancer cell SGC-7901 and regulation of Akt signaling way induced by bovine lactoferrin. J. Dairy Sci 2010, 93:2344-2350.
37. Yamada Y., Sato R., Kobayashi S., Hankanga C., Inanami O., Kuwabara M., Momota Y., Tomizawa N., Yasuda J. The antiproliferative effect of bovine lactoferrin on canine mammary gland tumor cells. J. Vet. Med. Sci. 2008, 70:443-448.
38. Yamauchi K., Toida T., Nishimura S., Nagano E., Kusuoka O., Teraguchi S., Hayasawa H., Shimamura S., Tomita M. 13-Week oral repeated administration toxicity study of bovine lactoferrin in rats. Food Chem. Toxicol. 2000, 38:503-512.
39. Yang C.S., Wang X. Green tea and cancer prevention. Nutr. Cancer. 2010, 62:931-937.
40. Yen C.C., Lin C.Y., Chong K.Y., Tsai T.C., Shen C.J., Lin M.F., Su C.Y., Chen H.L., Chen C.M. Lactoferrin as a natural regimen of selective decontamination of the digestive tract: Recombinant porcine lactoferrin expressed in the milk of transgenic mice protects neonates from pathogen challenges in the gastrointestinal tract. J. Infect. Dis. 2009, 199:590-598.
41. Yoo Y.C., Watanabe S., Watanabe R., Hata K., Shimazaki K., Azuma I. Bovine lactoferrin and lactoferricin, a peptide derived from bovine lactoferrin, inhibit tumor metastasis in mice. Jpn. J. Cancer Res 1997, 88:184-190.