Human apo-lactoferrin as a physiological mimetic of hypoxia stabilizes hypoxia-inducible factor-1 alpha

BioMetals

Volumn 25, Issue 6, 2012, Pages 1247-1259

  Zakharova, Elena T ^a   Kostevich, Valeria A ^a   Sokolov, Alexey V ^a   Vasilyev, Vadim B ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Russian Federation)

Author keywords

Ceruloplasmin; Desferoxamin; Erythropoietin; Hypoxia inducible factor 1 alpha; Iron chelator; Lactoferrin; Transferrin

Indexed keywords

APO LACTOFERRIN; CERULOPLASMIN; DEFEROXAMINE; ERYTHROPOIETIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LACTOFERRIN; UNCLASSIFIED DRUG;

ACUTE HYPOXIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN; CONTROLLED STUDY; HEART; HYPERCAPNIA; HYPOXIA; KIDNEY; LIVER; LUNG; MOUSE; NONHUMAN; PROTEIN STABILITY; PROTEIN TARGETING; SPLEEN; SURVIVAL TIME; SYNTHESIS; WESTERN BLOTTING;

ANOXIA; APOPROTEINS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LACTOFERRIN;

ANIMALIA; MUS;

EID: 84874107679     PISSN: 09660844     EISSN: 15728773     Source Type: Journal    
DOI: 10.1007/s10534-012-9586-y     Document Type: Article

References (100)

1. Aisen P, Harris DC (1989) Physical biochemistry of the transferrins. In: Loehr T (ed) Iron carriers and iron proteins, vol 5. VCH, New York, pp 241-351
2. Aisen P, Listowsky I (1980) Iron transport and storage proteins. Annu Rev Biochem 49:357-393
3. Anderson NL, Nance SL, Pearson TW et al (1982) Specific antiserun staining of two-dimensional electrophoretic patterns of human plasma proteins immobilized on nitricellulose. Electrophoresis 3:135-142
4. 3+) and zinc in the hippocampus. Brain Res 892:51-62
5. Bae MK, Ahn MY, Jeong JW et al (2002) Jab1 interacts directly with HIF-1alpha and regulates its stability. J Biol Chem 277:9-12
6. Baker EN (1994) Structure and reactivity of transferrins. Adv Inorg Chem 41:389-463
7. Ben-Shachar D, Eshel G, Riederer P et al (1992) Role of iron and iron chelation in dopaminergic-induced neurodegeneration: implication for Parkinson's disease. Ann Neurol 32:S105-S110
8. Birgens HS (1994) The monocytic receptor for lactoferrin and its involvement in lactoferrin-mediated iron transport. Adv Exp Med Biol 357:99-109
9. Botusan IR, Sunkari VG, Savu O et al (2008) Stabilization of HIF-1alpha is critical to improve wound healing in diabetic mice. Proc Natl Acad Sci USA 105:19426-19431
10. Brandl N, Zemann A, Kaupe I et al (2010) Signal transduction and metabolism in chondrocytes is modulated by lactoferrin. Osteoarthr Cartil 18:117-125
11. Brock JH (2002) The physiology of lactoferrin. Biochem Cell Biol 80:1-6
12. Budde A, Schneiderhan-Marra N, Petersen G et al (2005) Retinoblastoma susceptibility gene product pRB activates hypoxia-inducible factor-1 (HIF-1). Oncogene 24:1802-1808
13. Cario H, Janka-Schaub G, Janssen G et al (2007) Recent developments in iron chelation therapy. Klin Padiatr 219:158-165
14. Castellani RJ, Smith MA, Nunomura A et al (1999) Is increased redox-active iron in Alzheimer disease a failure of the copper-binding protein ceruloplasmin? Free Radic Biol Med 26:1508-1512
15. Chen-Roetling J, Chen L, Regan RF (2011) Apotransferrin protects cortical neurons from hemoglobin toxicity. Neuropharmacology 60:423-431
16. Cornish J, Callon KE, Naot D et al (2004) Lactoferrin is a potent regulator of bone cell activity and increases bone formation in vivo. Endocrinology 145:4366-4374
17. Damiens E, El Yazidi I, Mazurier J et al (1999) Lactoferrin inhibits G1 cyclin-dependent kinases during growth arrest of human breast carcinoma cells. J Cell Biochem 74:486-498
18. De Domenico I, Ward DM, Kaplan J (2009) Specific iron chelators determine the route of ferritin degradation. Blood 114:4546-4551
19. Dendorfer A, Heidbreder M, Hellwig-Bürgel T et al (2005) Deferoxamine induces prolonged cardiac preconditioning via accumulation of oxygen radicals. Free Radic Biol Med 38:117-124
20. Dhennin-Duthille I, Masson M, Damiens E et al (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
21. Ding JY, Kreipke CW, Schafer P et al (2009) Synapse loss regulated by matrix metalloproteinases in traumatic brain injury is associated with hypoxia inducible factor-1alpha expression. Brain Res 1268:125-134
22. Duce JA, Tsatsanis A, Cater MA et al (2010) Iron-export ferroxidase activity of β-amyloid precursor protein is inhibited by zinc in Alzheimer's disease. Cell 142:857-867
23. Elvidge GP, Glenny L, Appelhoff RJ et al (2006) Concordant regulation of gene expression by hypoxia and 2-oxoglutarate-dependent dioxygenase inhibition: the role of HIF-1alpha, HIF-2alpha, and other pathways. J Biol Chem 281:15215-15226
24. Engelmayer J, Blezinger P, Varadhachary A (2008) Talactoferrin stimulates wound healing with modulation of inflammation. J Surg Res 149:278-286
25. Fillebeen C, Descamps L, Dehouck MP et al (1999) Receptormediated transcytosis of lactoferrin through the bloodbrain barrier. J Biol Chem 274:7011-7017
26. Fling SP, Gregerson DS (1986) Peptide and protein molecular weight determination by electrophoresis using a highmolarity tris buffer system without urea. Anal Biochem 155:83-88
27. Forsythe JA, Jiang BH, Iyer NV et al (1996) Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 16:4604-4613
28. Fransson GB, Lonnerdal B (1980) Iron in human milk. J Pediatr 96:380-384
29. Frenkel-Denkberg G, Gershon D, Levy AP (1999) The function of hypoxia-inducible factor 1 (HIF-1) is impaired in senescent mice. FEBS Lett 462:341-344
30. Glezer I, Chernomoretz A, David S et al (2007) Genes involved in the balance between neuronal survival and death during inflammation. PLoS ONE 2:e310
31. He J, Furmanksi P (1995) Sequence specificity and transcriptional activation in the binding lactoferrin to DNA. Nature 373:721-724
32. Hellwig-Bürgel T, Rutkowski K, Metzen E et al (1999) Interleukin-1beta and tumor necrosis factor-alpha stimulate DNA binding of hypoxia-inducible factor-1. Blood 94:1561-1567
33. Hirsilä M, Koivunen P, Xu L et al (2005) Effect of desferrioxamine and metals on the hydroxylases in the oxygen sensing pathway. FASEB J 19:1308-1310
34. Hoke EM, Maylock CA, Shacter E (2005) Desferal inhibits breast tumor growth and does not interfere with the tumoricidal activity of doxorubicin. Free Radic Biol Med 39:403-411
35. Jewell UR, Kvietikova I, Scheid A et al (2001) Induction of HIF-1alpha in response to hypoxia is instantaneous. FASEB J 15:1312-1314
36. Jiang Y, Dai A, Li Q et al (2007) Hypoxia induces transforming growth factor-beta1 gene expression in the pulmonary artery of rats via hypoxia-inducible factor-1alpha. Acta Biochim Biophys Sin 39:73-80
37. Kamemori N, Takeuchi T, Sugiyama A et al (2008) Transendothelial and trans-epithelial transfer of lactoferrin into the brain through BBB and BCSFB in adult rats. J Vet Med Sci 70:313-315
38. Keberle H (1964) The biochemistry of desferrioxamine and its relation to iron metabolism. Ann N Y Acad Sci 119: 758-775
39. Kim CW, Son KN, Choi SY et al (2006) Human lactoferrin upregulates expression of KDR/Flk-1 and stimulates VEGF-A-mediated endothelial cell proliferation and migration. FEBS Lett 580:4332-4336
40. Knowles HJ, Raval RR, Harris AL et al (2003) Effect of ascorbate on the activity of hypoxia-inducible factor in cancer cells. Cancer Res 63:1764-1768
41. Kontoghiorghes GJ, Kolnagou A, Skiada A et al (2010) The role of iron and chelators on infections in iron overload and non iron loaded conditions: prospects for the design of new antimicrobial therapies. Hemoglobin 34:227-239
42. Kovacevic Z, Kalinowski DS, Lovejoy DB et al (2011) The medicinal chemistry of novel iron chelators for the treatment of cancer. Curr Top Med Chem 11:483-499
43. Kozu T, Iinuma G, Ohashi Y et al (2009) Effect of orally administered bovine lactoferrin on the growth of adenomatous colorectal polyps in a randomized, placebocontrolled clinical trial. Cancer Prev Res 2:975-983
44. Kruzel ML, Actor JK, Radak Z et al (2010) Lactoferrin decreases LPS-induced mitochondrial dysfunction in cultured cells and in animal endotoxemia model. Innate Immun 16:67-79
45. Lakhal S, Talbot NP, Crosby A et al (2009) Regulation of growth differentiation factor 15 expression by intracellular iron. Blood 113:1555-15563
46. Larsen M, Høg A, Lund EL et al (2005) Interactions between HIF-1 and Jab1: balancing apoptosis and adaptation. Outline of a working hypothesis. Adv Exp Med Biol 566:203-211
47. Lee JW (2008) Iron chelation therapy in the myelodysplastic syndromes and aplastic anemia: a review of experience in South Korea. Int J Hematol 88:16-23
48. Lee JW, Bae SH, Jeong JW et al (2004) Hypoxia-inducible factor (HIF-1)alpha: its protein stability and biological functions. Exp Mol Med 36:1-12
49. Li L, Frei B (2006) Iron chelation inhibits NF-kappa B-mediated adhesion molecule expression by inhibiting p22(phox) protein expression and NADPH oxidase activity. Arterioscler Thromb Vasc Biol 26:2638-2643
50. Liao Y, Jiang R, Lönnerdal B (2012) Biochemical and molecular impacts of lactoferrin on small intestinal growth and development during early life. Biochem Cell Biol 90(3):476-484
51. Lopez V, Kelleher SL, Lonnerdal B (2008) Lactoferrin receptor mediates apo-but not holo-lactoferrin internalization via clathrin-mediated endocytosis in trophoblasts. Biochem J 411:271-278
52. Lyons TE, Miller MS, Serena T et al (2007) Talactoferrin alfa, a recombinant human lactoferrin promotes healing of diabetic neuropathic ulcers: a phase 1/2 clinical study. Am J Surg 193:49-54
53. Manning T, Kean G, Thomas J et al (2009) Iron chelators in medicinal applications-chemical equilibrium considerations in pharmaceutical activity. Curr Med Chem 16:2416-2429
54. Masson PL (1970) La lactoferrine. Proteine des secretions externes et des leucocytes neutrophiles. Editions Arscia S.A., Brussels
55. Mazurier J, Spik G (1980) Comparative study of the ironbinding properties of human transferrins. I. Complete and sequential iron saturation and desaturation of the lactotransferrin. Biochim Biophys Acta 629:399-408
56. Mizuno S, Bogaard HJ, Voelkel NF et al (2009) Hypoxia regulates human lung fibroblast proliferation via p53-dependent and-independent pathways. Respir Res 10:17
57. Mukhopadhyay CK, Mazumder B, Fox PL (2000) Role of hypoxia-inducible factor-1 in transcriptional activation of ceruloplasmin by iron deficiency. J Biol Chem 275:21048-21054
58. Mulligan P, White NR, Monteleone G et al (2006) Breast milk lactoferrin regulates gene expression by binding bacterial DNA CpG motifs but not genomic DNA promoters in model intestinal cells. Pediatr Res 59:656-661
59. Nakajima KI, Kanno Y, Nakamura M et al (2011) Bovine milk lactoferrin induces synthesis of the angiogenic factors VEGF and FGF2 in osteoblasts via the p44/p42 MAP kinase pathway. Biometals 24:847-856
60. Naot D, Chhana A, Matthews BG et al (2011) Molecular mechanisms involved in the mitogenic effect of lactoferrin in osteoblasts. Bone 49:217-224
61. Ndubuizu OI, Chavez JC, La Manna JC (2009) Increased prolyl 4-hydroxylase expression and differential regulation of hypoxia-inducible factors in the aged rat brain. Am J Physiol Regul Integr Comp Physiol 297:R158-R165
62. Nichols BL, McKee KS, Huebers HA (1990) Iron is not required in the lactoferrin stimulation of thymidine incorporation into the DNA of rat crypt enterocytes. Pediatr Res 27:525-528
63. Norrby K (2004) Human apo-lactoferrin enhances angiogenesis mediated by vascular endothelial growth factor A in vivo. J Vasc Res 41:293-304
64. Nowicki M, Kosacka J, Spanel-Borowski K et al (2009) Deferoxamine-induced neurite outgrowth and synapse formation in postnatal rat dorsal root ganglion (DRG) cell cultures. Eur J Cell Biol 88:551-562
65. Oh SM, Hahm DH, Kim IH et al (2001) Human neutrophil lactoferrin trans-activates the matrix metalloproteinase 1 gene through stress-activated MAPK signaling modules. J Biol Chem 276:42575-42579
66. Oh SM, Pyo CW, Kim Y et al (2004) Neutrophil lactoferrin upregulates the human p53 gene through induction of NF kappaB activation cascade. Oncogene 23:8282-8291
67. Paesano R, Berlutti F, Pietropaoli M et al (2010) Lactoferrin efficacy versus ferrous sulfate in curing iron disorders in pregnant and non-pregnant women. Int J Immunopathol Pharmacol 23:577-587
68. Parodi PW (2007) A role for milk proteins and their peptides in cancer prevention. Curr Pharm Des 13:813-828
69. Pedchenko TV, LeVine SM (1998) Desferrioxamine suppresses experimental allergic encephalomyelitis induced by MBP in SJL mice. J Neuroimmunol 84:188-197
70. Peden DB, Brown ME, Wade Y et al (1991) Human nasal glandular secretion of novel antioxidant activity: cholinergic control. Am Rev Respir Dis 143:545-552
71. Piperno A, Galimberti S, Mariani R et al (2011) Modulation of hepcidin production during hypoxia-induced erythropoiesis in humans in vivo: data from the HIGHCARE project. Blood 117:2953-2959
72. Pulina MO, Sokolov AV, Zakharova ET et al (2010) Effect of lactoferrin on consequences of acute experimental hemorrhagic anemia in rats. Bull Exp Biol Med 149:219-222
73. Ren X, Dorrington KL, Maxwell PH et al (2000) Effect of desferrioxamine on serum erythropoietin and ventilator sensitivity to hypoxia in humans. J Appl Physiol 89:680-686
74. Richard DE, Berra E, Gothié E et al (1999) p42/p44 mitogenactivated protein kinases phosphorylate hypoxia-inducible factor 1alpha (HIF-1alpha) and enhance the transcriptional activity of HIF-1. J Biol Chem 274:32631-32637
75. Saletta F, Rahmanto YS, Noulsri E et al (2010) Iron chelatormediated alterations in gene expression: identification of novel iron-regulated molecules that are molecular targets of hypoxia-inducible factor-1 alpha and p53. Mol Pharmacol 77:443-458
76. Salvador GA, Uranga RM, Giusto NM (2010) Iron and mechanisms of neurotoxicity. Int J Alzheimers Dis 2011:720658
77. Seifert A, Rau S, Küllertz G et al (2009) TCDD induces cell migration via NFA Tc1/ATX-signaling in MCF-7 cells. Toxicol Lett 184:26-32
78. Semenza GL (2010) Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics. Oncogene 29:625-634
79. Shoji H, Oguchi S, Shinohara K et al (2007) Effects of ironunsaturated human lactoferrin on hydrogen peroxideinduced oxidative damage in intestinal epithelial cells. Pediatr Res 61:89-92
80. Smith DG, Cappai R, Barnham KJ (2007) The redox chemistry of the Alzheimer's disease amyloid beta peptide. Biochim Biophys Acta 1768:1976-1990
81. Sokolov AV, Zakharova ET, Shavlovskii MM et al (2005) Isolation of stable human ceruloplasmin and its interaction with salmon protamine. Bioorg Khim 31:269-279
82. Sokolov AV, Ageeva KV, Pulina MO et al (2009) Effect of lactoferrin on oxidative features of ceruloplasmin. Biometals 22:521-529
83. Sokolov AV, Solovyev KV, Kostevich VA et al (2012) Protection of ceruloplasmin by lactoferrin against hydroxyl radicals is pH dependent. Biochem Cell Biol 90(3):397-404
84. Son K-N, Park J, Chung C-K et al (2002) Human lactoferrin activates transcription of IL-1β gene in mammalian cells. Biochem Biophys Res Commun 290:236-241
85. Son HJ, Lee SH, Choi SY (2006) Human lactoferrin controls the level of retinoblastoma protein and its activity. Biochem Cell Biol 84:345-350
86. Spik G, Brunet B, Mazurier-Dehaine C et al (1982) Characterization and properties of the human and bovine lactotransferrins extracted from the faeces of newborn infants. Acta Paediatr Scand 71:979-985
87. Tafani M, Russo A, Di Vito Met al (2010) Up-regulation of proinflammatory genes as adaptation to hypoxia in MCF-7 cells and in human mammary invasive carcinoma microenvironment. Cancer Sci 101:1014-1023
88. Tanno T, Bhanu NV, Oneal PA et al (2007) High levels of GDF15 in thalassemia suppress expression of the iron regulatory protein hepcidin. Nat Med 13:1096-1101
89. Teng CT (2002) Lactoferrin gene expression and regulation: an overview. Biochem Cell Biol 80:7-16
90. Thangarajah H, Vial IN, Grogan RH et al (2010) HIF-1alpha dysfunction in diabetes. Cell Cycle 9:75-79
91. Troost FJ, Steijns J, Saris WH et al (2001) Gastric digestion of bovine lactoferrin in vivo in adults. J Nutr 131:2101-2104
92. Tsuda H, Kozu T, Iinuma G et al (2010) Cancer prevention by bovine lactoferrin: from animal studies to human trial. Biometals 23:399-409
93. Ueno M, Maeno T, Nomura M et al (2011) Hypoxia-inducible factor-1α mediates TGF-β-induced PAI-1 production in alveolar macrophages in pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 300:L740-L752
94. Vaithilingam V, Oberholzer J, Guillemin GJ et al (2010) Beneficial effects of desferrioxamine on encapsulated human islets-in vitro and in vivo study. Am J Transpl 10:1961-1969
95. Wan C, Gilbert SR, Wang Y et al (2008) Activation of the hypoxia-inducible factor-1alpha pathway accelerates bone regeneration. Proc Natl Acad Sci U S A 105:686-691
96. Wan C, Shao J, Gilbert SR et al (2010) Role of HIF-1alpha in skeletal development. Ann N Y Acad Sci 1192:322-326
97. Wang GL, Semenza GL (1993) Desferrioxamine induces erythropoietin gene expression and hypoxia-inducible factor 1 DNA-binding activity: implications for models of hypoxia signal transduction. Blood 82:3610-3615
98. Whitnall M, Howard J, Ponka P et al (2006) A class of iron chelators with a wide spectrum of potent antitumor activity that overcomes resistanse to chemotherapeutics. PNAS 103:14901-14906
99. Zhou G, Dada LA, Wu Met al (2009) Hypoxia-induced alveolar epithelial-mesenchymal transition requires mitochondrial ROS and hypoxia-inducible factor 1. Am J Physiol Lung Cell Mol Physiol 297:L1120-L1130
100. Zimecki M, Kocieba M, Chodaczek G et al (2007) Lactoferrin ameliorates symptoms of experimental encephalomyelitis in Lewis rats. J Neuroimmunol 182:160-166