Bovine lactoferrin induces cell cycle arrest and inhibits mtor signaling in breast cancer cells

Nutrition and Cancer

Volumn 66, Issue 8, 2014, Pages 1371-1385

  Zhang, Yunlei ^a   Nicolau, Ana ^a   Lima, Cristovao F ^a   Rodrigues, Lígia R ^a  

^a UNIVERSITY OF MINHO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

IRON; LACTOFERRIN; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHOTHREONINE; ANTINEOPLASTIC AGENT; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MTOR PROTEIN, HUMAN; TARGET OF RAPAMYCIN KINASE;

APOPTOSIS; ARTICLE; BREAST CANCER; BREAST CANCER CELL LINE; CANCER CELL; CANCER CELL LINE; CANCER RESEARCH; CELL CYCLE ARREST; CONTROLLED STUDY; CULTURE MEDIUM; CYTOTOXICITY; ENERGY; INTERNALIZATION; MOLECULAR MECHANICS; NUTRIENT; SIGNAL TRANSDUCTION; ANIMAL; BOVINE; BREAST TUMOR; CELL CYCLE CHECKPOINT; DOWN REGULATION; DRUG EFFECTS; FEMALE; GENETICS; HUMAN; MCF 7 CELL LINE; METABOLISM; PHOSPHORYLATION; TUMOR CELL LINE;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BREAST NEOPLASMS; CATTLE; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; DOWN-REGULATION; FEMALE; HUMANS; LACTOFERRIN; MCF-7 CELLS; PHOSPHORYLATION; TOR SERINE-THREONINE KINASES;

EID: 84911395117     PISSN: 01635581     EISSN: 15327914     Source Type: Journal    
DOI: 10.1080/01635581.2014.956260     Document Type: Article

References (72)

1. Milner JA: Molecular targets for bioactive food components. J Nutr 134, 2492S-2498S, 2004.
2. Patel B, Das S, and Prakash R: Natural bioactive compound with anticancer potential. Int J Adv Pharm Sci 1, 32-41, 2010.
3. Young SK and Milner JA: Bioactive food components and cancer-specific metabonomic profiles. J Biomed Biotechnol. Advanced online publication. doi: http://dx.doi.org/10.1155%2F2011%2F721213.2011.
4. Dennis T, Fanous M, and Mousa S: Natural products for chemopreventive and adjunctive therapy in oncologic disease. Nutr Cancer 61, 587-597, 2009.
5. Pan MH, Lai CS, Tsai ML, Wu JC, and Ho CT: Molecular mechanisms for anti-aging by natural dietary compounds. Mol Nutr Food Res 56, 88-115, 2012.
6. Adlerova L, Bartoskova A, and Faldyna M: Lactoferrin: a review. Veterinarni Medicina 53, 457-468, 2008.
7. Ushida Y, Sekine K, Kuhara T, Takasuka N, Iigo M, et al.: Possible Chemopreventive Effects of Bovine Lactoferrin on Esophagus and Lung Carcinogenesis in the Rat. Jpn J Cancer Res 90, 262-267, 1999.
8. Kuhara T, Iigo M, Itoh T, Ushida Y, Sekine K, et al.: Orally administered Lactoferrin exerts an antimetastatic effect and enhances production of IL- 18 in the Intestinal epithelium. Nutr Cancer 38, 192-199, 2000.
9. Xiao Y, Monitto CL, Minhas KM, and Sidransky D: Lactoferrin downregulates G1 cyclin-dependent kinases during growth arrest of head and neck cancer cells. Clin Cancer Res 10, 8683-8686, 2004.
10. Chandra Mohan KV, Kumaraguruparan R, Prathiba D, and Nagini S: Modulation of xenobiotic-metabolizing enzymes and redox status during chemoprevention of hamster buccal carcinogenesis by bovine lactoferrin. Nutrition 22, 940-946, 2006.
11. Tomita M, Wakabayashi H, Yamauchi K, Teraguchi S, and Hayasawa H: Bovine lactoferrin and lactoferricin derived from milk: production and applications. Biochem Cell Biol 80, 109-112, 2002.
12. Rodrigues L, Teixeira J, Schmitt F, Paulsson M, and Månsson HL: Lactoferrin and cancer disease prevention. Crit Rev Food Sci Nutr 49, 203-217, 2009.
13. Tsuda H, Kozu T, Iinuma G, Ohashi Y, Saito Y, et al.: Cancer prevention by bovine lactoferrin: from animal studies to human trial. Biometals 23, 399-409, 2010.
14. Roy MK, Kuwabara Y, Hara K, Watanabe Y, and Tamai Y: Peptides from the N-terminal end of bovine lactoferrin induce apoptosis in human leukemic (HL-60) cells. J Dairy Sci 85, 2065-2074, 2002.
15. Onishi J, Roy MK, Juneja LR, Watanabe Y, and Tamai Y: A lactoferrinderived peptide with cationic residues concentrated in a region of its helical structure induces necrotic cell death in a leukemic cell line (HL-60). J Pept Sci 14, 1032-1038, 2008.
16. Fillebeen C, Descamps L, Dehouck MP, Fenart L, Benaïssa M, et al.: Receptor-mediated transcytosis of lactoferrin through the blood-brain barrier. J Biol Chem 274, 7011-7017, 1999.
17. Jiang R, Lopez V, Kelleher SL, and Lönnerdal B: Apo- and holo-lactoferrin are both internalized by lactoferrin receptor via clathrin-mediated endocytosis but differentially affect ERK-signaling and cell proliferation in Caco-2 cells. J Cell Physiol 226, 3022-3031, 2011.
18. Rochard E, Legrand D, Lecocq M, Hamelin R, Crepin M, et al.: Characterization of lactotransferrin receptor in epithelial cell lines from nonmalignant human breast, benign mastopathies and breast carcinomas. Anticancer Res 12, 2047-2051, 1992.
19. Bi BY, Liu JL, Legrand D, Roche AC, Capron M, et al.: Internalization of human lactoferrin by the Jurkat human lymphoblastic T-cell line. Eur J Cell Biol 69, 288-296, 1996.
20. Damiens E, Mazurier J, el Yazidi I, Masson M, Duthille I, et al.: Effects of human lactoferrin on NK cell cytotoxicity against haematopoietic and epithelial tumour cells. Biochim Biophys Acta 1402, 277-287, 1998.
21. Lin TY, Chiou SH, Chen M, and Kuo CD: Human lactoferrin exerts bidirectional actions on PC12 cell survival via ERK1/2 pathway. Biochem Biophys Res Commun 337, 330-336, 2005.
22. Zhou Y, Zeng Z, Zhang W, Xiong W, Wu M, et al.: Lactotransferrin: a candidate tumor suppressor-deficient expression in human nasopharyngeal carcinoma and inhibition of NPC cell proliferation by modulating the mitogen-activated protein kinase pathway. Int J Cancer 123, 2065-2072, 2008.
23. Xu XX, Jiang HR, Li HB, Zhang TN, Zhou Q, et al.: Apoptosis of stomach cancer cell SGC-7901 and regulation of Akt signaling way induced by bovine lactoferrin. J Dairy Sci 93, 2344-2350, 2010.
24. Damiens E, El Yazidi I, Mazurier J, Duthille I, Spik G, et al.: Lactoferrin inhibits G1 cyclin-dependent kinases during growth arrest of human breast carcinoma cells. J Cell Biochem 74, 486-498, 1999.
25. Sakai T, Banno Y, Kato Y, Nozawa Y, and Kawaguchi M: Pepsindigested bovine lactoferrin induces apoptotic cell death with JNK/SAPK activation in oral cancer cells. J Pharmacol Sci 98, 41-48, 2005.
26. Furlong SJ, Mader JS, and Hoskin DW: Lactoferricin-induced apoptosis in estrogen-nonresponsive MDA-MB-435 breast cancer cells is enhanced by C6 ceramide or tamoxifen. Oncol Rep 15, 1385-1390, 2006.
27. Lee SH, Park SW, Pyo CW, Yoo NK, Kim J, et al.: Requirement of the JNK-associated Bcl-2 pathway for human lactoferrin-induced apoptosis in the Jurkat leukemia T cell line. Biochimie 91, 102-108, 2009.
28. Duarte DC, Nicolau A, Teixeira JA, and Rodrigues LR: The effect of bovine milk lactoferrin on human breast cancer cell lines. J Dairy Sci 94, 66-76, 2011.
29. Furmanski P, Li ZP, Fortuna MB, Swamy CV, and Das MR: Multiple molecular forms of human lactoferrin. Identification of a class of lactoferrins that possess ribonuclease activity and lack iron-binding capacity. J Exp Med 170, 415-429, 1989.
30. Siebert PD and Huang BC: Identification of an alternative form of human lactoferrin mRNA that is expressed differentially in normal tissues and tumor-derived cell lines. Proc Natl Acad Sci U S A 94, 2198-2203, 1997.
31. Hoedt E, Hardivillé S, Mariller C, Elass E, Perraudin JP, et al.: Discrimination and evaluation of lactoferrin and delta-lactoferrin gene expression levels in cancer cells and under inflammatory stimuli using TaqMan realtime PCR. Biometals 23, 441-452, 2010.
32. Breton M, Mariller C, Benaïssa M, Caillaux K, Browaeys E, et al.: Expression of delta-lactoferrin induces cell cycle arrest. Biometals 17, 325-329, 2004.
33. O'Connor PM, Jackman J, Bae I, Myers TG, Fan S, et al.: Characterization of the p53 tumor suppressor pathway in cell lines of the National Cancer Institute anticancer drug screen and correlations with the growthinhibitory potency of 123 anticancer agents. Cancer Res 57, 4285-4300, 1997.
34. Weigel RJ and deConinck EC: Transcriptional control of estrogen receptor in estrogen receptor-negative breast carcinoma. Cancer Res 53, 3472-3474, 1993.
35. Ford CH, Al-Bader M, Al-Ayadhi B, and Francis I: Reassessment of estrogen receptor expression in human breast cancer cell lines. Anticancer Res 31, 521-527, 2011.
36. Soule HD, Maloney TM, Wolman SR, Peterson WD Jr, Brenz R, et al.: Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF10. Cancer Res 50, 6075-6086, 1990.
37. Hackett AJ, Smith HS, Springer EL, Owens RB, Nelson-Rees WA, et al.: Two syngeneic cell lines from human breast tissue: the aneuploid mammary epithelial (Hs578T) and the diploid myoepithelial (Hs578Bst) cell lines. J Natl Cancer Inst, 58, 1795-1806, 1977.
38. Schägger H: Tricine-SDS-PAGE. Nat Protoc 1, 16-22, 2006.
39. Xavier CP, Lima CF, Fernandes-Ferreira M, and Pereira-Wilson C: Salvia fruticosa, Salvia officinalis, and rosmarinic acid induce apoptosis and inhibit proliferation of human colorectal cell lines: the role in MAPK/ ERK pathway. Nutr Cancer 61, 564-571, 2009.
40. Kanwar JR, Palmano KP, Sun X, Kanwar RK, Gupta R, et al.: 'Iron-saturated' lactoferrin is a potent natural adjuvant for augmenting cancer chemotherapy. Immunol Cell Biol 86, 277-288, 2008.
41. Li S, Zhou H, Huang G, and Liu N: Inhibition of HBV infection by bovine lactoferrin and iron-, zinc-saturated lactoferrin. Med Microbiol Immunol 198, 19-25, 2009.
42. Foley AA, Bates GW: The purification of lactoferrin from human whey by batch extraction. Anal Biochem 162, 296-300, 1987.
43. Yang N, Lejon T, and Rekdal O: Antitumour activity and specificity as a function of substitutions in the lipophilic sector of helical lactoferrinderived peptide. J Pept Sci 9, 300-311, 2003.
44. Duchardt F, Ruttekolk IR, Verdurmen WP, Lortat-Jacob H, Bürck J, et al.: A cell-penetrating peptide derived from human lactoferrin with conformation-dependent uptake efficiency. J Biol Chem 284, 36099-36108, 2009.
45. Freiburghaus C, Janicke B, Lindmark-Månsson H, Oredsson S, and Paulsson MA: Lactoferricin treatment decreases the rate of cell proliferation of a human colon cancer cell line. J Dairy Sci 92, 2477-2484, 2009.
46. Yang N, Stensen W, Svendsen JS, and Rekdal Ø: Enhanced antitumor activity and selectivity of lactoferrin-derived peptides. J Pept Res 60, 187-197, 2002.
47. Zhang TN, Yang W, and Liu N: Effect of loop structure of bovine lactoferricin on apoptosis in Jurkat cells. Biometals 23, 555-561, 2010.
48. Cai B, Chang SH, Becker EB, Bonni A, and Xia Z: p38 MAP kinase mediates apoptosis through phosphorylation of BimEL at Ser-65. J Biol Chem 281, 25215-25222, 2006.
49. Worster DT, Schmelzle T, Solimini NL, Lightcap ES, Millard B, et al.: Akt and ERK control the proliferative response of mammary epithelial cells to the growth factors IGF-1 and EGF through the cell cycle inhibitor p57Kip2. Sci Signal 5, ra19, 2012.
50. Tokunaga C, Yoshino K, and Yonezawa K: mTOR integrates amino acidand energy-sensing pathways. Biochem Biophys Res Commun 313, 443-446, 2004.
51. Morgensztern D and McLeod HL: PI3K/Akt/mTOR pathway as a target for cancer therapy. Anticancer Drugs 16, 797-803, 2005.
52. Vollenbröker B, George B, Wolfgart M, Saleem MA, Pavenstädt H, et al.: mTOR regulates expression of slit diaphragm proteins and cytoskeleton structure in podocytes. Am J Physiol Renal Physiol 296, F418-F426, 2009.
53. Johnson SM, Gulhati P, Arrieta I, Wang X, Uchida T, et al.: Curcumin inhibits proliferation of colorectal carcinoma by modulating Akt/mTOR signaling. Anticancer Res 29, 3185-3190, 2009.
54. Noh WC, Mondesire WH, Peng J, Jian W, Zhang H, et al.: Determinants of rapamycin sensitivity in breast cancer cells. Clin Cancer Res 10, 1013-1023, 2004.
55. Shackelford DB and Shaw RJ: The LKB1-AMPK pathway: metabolism and growth control in tumour suppression. Nat Rev Cancer 9, 563-575, 2009.
56. Tamura K, Southwick EC, Kerns J, Rosi K, Carr BI, et al.: Cdc25 inhibition and cell cycle arrest by a synthetic thioalkyl vitamin K analogue. Cancer Res 60, 1317-1325, 2000.
57. Sun X, Jiang R, Przepiorski A, Reddy S, Palmano KP, et al.: "Iron-saturated" bovine lactoferrin improves the chemotherapeutic effects of tamoxifen in the treatment of basal-like breast cancer in mice. BMC Cancer 12, 591, 2012.
58. Baker EN and Baker HM: A structural framework for understanding the multifunctional character of lactoferrin. Biochimie 91, 3-10, 2009.
59. Link G, Saada A, Pinson A, Konijn AM, and Hershko C: Mitochondrial respiratory enzymes are a major target of iron toxicity in rat heart cells. J Lab Clin Med 131, 466-474. 1998.
60. He WL, Feng Y, Li XL, Wei YY, and Yang XE: Availability and toxicity of Fe(II) and Fe(III) in Caco-2 cells. J Zhejiang Univ Sci B 9, 707-712, 2008.
61. Yamada Y, Sato R, Kobayashi S, Hankanga C, Inanami O, et al.: The antiproliferative effect of bovine lactoferrin on canine mammary gland tumor cells. J Vet Med Sci 70, 443-448, 2008.
62. Dasika GK, Lin SC, Zhao S, Sung P, Tomkinson A, et al.: DNA damageinduced cell cycle checkpoints and DNA strand break repair in development and tumorigenesis. Oncogene 18, 7883-7899, 1999.
63. Igney FH and Krammer PH: Immune escape of tumors: apoptosis resistance and tumor counterattack. J Leukoc Biol 71, 907-920, 2002.
64. Gasco M, Shami S, and Crook T: The p53 pathway in breast cancer. Breast Cancer Res 4, 70-76, 2002.
65. Meulmeester E, Jochemsen AG: p53: a guide to apoptosis. Curr. Cancer Drug Tar 8, 87-97, 2008.
66. Jänicke RU: MCF-7 breast carcinoma cells do not express caspase-3. Breast Cancer Res Treat 117, 219-221, 2009.
67. Roy SK, Srivastava RK, and Shankar S: Inhibition of PI3K/AKT and MAPK/ERK pathways causes activation of FOXO transcription factor, leading to cell cycle arrest and apoptosis in pancreatic cancer. J Mol Signal 5, 10, 2010.
68. Kim J, Kundu M, Viollet B, and Guan KL: AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol 13, 132-141, 2011.
69. Mulder AM, Connellan PA, Oliver CJ, Morris CA, and Stevenson LM: Bovine lactoferrin supplementation supports immune and antioxidant status in healthy human males. Nutr Res 28, 583-589, 2008.
70. Wang YY and Malik R: Safety and Efficacy of Talactoferrin in Previously Treated Patients with Non-Small Cell Lung Cancer (FORTIS-M). Clinical trials, Gov. registration number: NCT00707304.
71. Wang YY and Malik R. Safety and Efficacy of Talactoferrin in Addition to Standard Chemotherapy in Patients with Non-Small Cell Lung Cancer (FORTIS-C). Clinical trials, Gov. registration number: NCT00706862.
72. Nozaki A, Ikeda M, Naganuma A, Nakamura T, and Inudoh M: Identification of a lactoferrin-derived peptide possessing binding activity to hepatitis C virus E2 envelope protein. J Biol Chem 278, 10162-10173, 2003.