Delta-lactoferrin, an intracellular lactoferrin isoform that acts as a transcription factor

Biochemistry and Cell Biology

Volumn 90, Issue 3, 2012, Pages 307-319

  Mariller, Christophe ^a   Hardivilĺ, Stephan ^a   Hoedt, Esthelle ^a   Huvent, Isabelle ^a   Pina Canseco, Socorro ^a   Pierce, Annick ^a  

^a UNIVERSITÉ DES SCIENCES ET TECHNOLOGIES DE LILLE   (France)

Author keywords

Antitumoral agent; Delta lactoferrin; Posttranslational modifications; Prognostic factor; Transcription factor

Indexed keywords

ANTIPROLIFERATIVE PROPERTIES; BREAST CANCER; CELL HOMEOSTASIS; CELL-CYCLE ARREST; CELLULAR HOMEOSTASIS; DELTA-LACTOFERRIN; EXPRESSION LEVELS; HEALTHY TISSUES; IN-VIVO; ISOFORMS; LACTOFERRIN; NUCLEOCYTOPLASMIC; POST-TRANSLATIONAL MODIFICATIONS; PROGNOSTIC FACTORS; RESPONSE ELEMENTS; SUMOYLATION; TARGET GENES; TRANSCRIPTIONAL ACTIVITY; UBIQUITINATION;

ACTIVATION ANALYSIS; DIAGNOSIS; DISEASES; GENES; PHOSPHORYLATION; PHYSIOLOGY; TISSUE;

TRANSCRIPTION FACTORS;

POLYPEPTIDE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DELTA LACTOFERRIN; UNCLASSIFIED DRUG;

ACYLATION; CELL CYCLE ARREST; CRYSTALLOGRAPHY; HOMEOSTASIS; HUMAN; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; REVIEW; SEQUENCE ANALYSIS; SUMOYLATION; UBIQUITINATION;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CONSENSUS SEQUENCE; GENE EXPRESSION REGULATION; HUMANS; LACTOFERRIN; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; PROTEIN ISOFORMS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SURFACE PROPERTIES; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84861363011     PISSN: 08298211     EISSN: 12086002     Source Type: Journal    
DOI: 10.1139/o11-070     Document Type: Review

References (82)

1. Aisen P. Leibman A. 1972. Lactoferrin and transferrin: a comparative study. Biochim. Biophys. Acta, 257 (2): 314-323. 4336719
2. Ambros V. 2004. The functions of animal microRNAs. Nature, 431 (7006): 350-355. 10.1038/nature02871 15372042
3. Anderson B.F. Baker H.M. Dodson E.J. Norris G.E. Rumball S.V. Waters J.M. Baker E.N. 1987. Structure of human lactoferrin at 3.2-Å resolution. Proc. Natl. Acad. Sci. U.S.A. 84 (7): 1769-1773. 10.1073/pnas.84.7.1769 3470756
4. Anderson B.F. Baker H.M. Norris G.E. Rice D.W. Baker E.N. 1989. Structure of human lactoferrin: crystallographic structure analysis and refinement at 2.8 Å resolution. J. Mol. Biol. 209 (4): 711-734. 10.1016/0022-2836(89)90602- 5 2585506
5. Bai C. Sen P. Hofmann K. Ma L. Goebl M. Harper J.W. Elledge S.J. 1996. SKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box. Cell, 86 (2): 263-274. 10.1016/S0092-8674(00) 80098-7 8706131
6. Baker E.N. 2005. Lactoferrin: a multi-tasking protein par excellence. Cell. Mol. Life Sci. 62 (22): 2529-2530. 10.1007/s00018-005-5366-y 16261258
7. Baker E.N. Baker H.M. 2009. A structural framework for understanding the multifunctional character of lactoferrin. Biochimie, 91 (1): 3-10. 10.1016/j.biochi.2008.05.006 18541155
8. Baker E.N. Baker H.M. Kidd R.D. 2002. Lactoferrin and transferrin: functional variations on a common structural framework. Biochem. Cell Biol. 80 (1): 27-34. 10.1139/o01-153 11908640
9. Baldwin G.S. 1993. Comparison of transferrin sequences from different species. Comp. Biochem. Physiol. B, 106 (1): 203-218. 10.1016/0305-0491(93) 90028-4 8403849
10. Baltimore D. Boldin M.P. O'Connell R.M. Rao D.S. Taganov K.D. 2008. MicroRNAs: new regulators of immune cell development and function. Nat. Immunol. 9 (8): 839-845. 10.1038/ni.f.209 18645592
11. Benaäraquo;ssa M. Peyrat J.-P. Hornez L. Mariller C. Mazurier J. Pierce A. 2005. Expression and prognostic value of lactoferrin mRNA isoforms in human breast cancer. Int. J. Cancer, 114 (2): 299-306. 10.1002/ijc.20728 15543612
12. Benayoun B.A. Veitia R.A. 2009. A post-translational modification code for transcription factors: sorting through a sea of signals. Trends Cell Biol. 19 (5): 189-197. 10.1016/j.tcb.2009.02.003 19328693
13. Breton M. Mariller C. Benaäraquo;ssa M. Caillaux K. Browaeys E. Masson M. et al. 2004. Expression of delta-lactoferrin induces cell cycle arrest. Biometals, 17 (3): 325-329. 10.1023/B:BIOM.0000027712.81056.13 15222485
14. Calvo S.E. Pagliarini D.J. Mootha V.K. 2009. Upstream open reading frames cause widespread reduction of protein expression and are polymorphic among humans. Proc. Natl. Acad. Sci. U.S.A. 106 (18): 7507-7512. 10.1073/pnas. 0810916106 19372376
15. Carrano A.C. Eytan E. Hershko A. Pagano M. 1999. SKP2 is required for ubiquitin-mediated degradation of the CDK inhibitor p27. Nat. Cell Biol. 1 (4): 193-199. 10.1038/12013 10559916
16. Carthew R.W. Sontheimer E.J. 2009. Origins and mechanisms of miRNAs and siRNAs. Cell, 136 (4): 642-655. 10.1016/j.cell.2009.01.035 19239886
17. Cheng X. Hart G.W. 2000. Glycosylation of the murine estrogen receptor-alpha. J. Steroid Biochem. Mol. Biol. 75 (2-3): 147-158. 10.1016/S0960-0760(00)00167-9 11226831
18. Comer F.I. Hart G.W. 2001. Reciprocity between O-GlcNAc and O-phosphate on the carboxyl terminal domain of RNA polymerase II. Biochemistry, 40 (26): 7845-7852. 10.1021/bi0027480 11425311
19. Desterro J.M. Rodriguez M.S. Hay R.T. 1998. SUMO-1 modification of IκBalphaα inhibits NF-κB activation. Mol. Cell, 2 (2): 233-239. 10.1016/S1097-2765(00)80133-1 9734360
20. Efthymiadis A. Shao H. Hübner S. Jans D.A. 1997. Kinetic characterization of the human retinoblastoma protein bipartite nuclear localization sequence (NLS) in vivo and in vitro. A comparison with the SV40 large T-antigen NLS. J. Biol. Chem. 272 (35): 22134-22139. 10.1074/jbc.272.35. 22134 9268357
21. Frischmeyer P.A. van Hoof A. O'Donnell K. Guerrerio A.L. Parker R. Dietz H.C. 2002. An mRNA surveillance mechanism that eliminates transcripts lacking termination codons. Science, 295 (5563): 2258-2261. 10.1126/science.1067338 11910109
22. Gareau J.R. Lima C.D. 2010. The SUMO pathway: emerging mechanisms that shape specificity, conjugation and recognition. Nat. Rev. Mol. Cell Biol. 11 (12): 861-871. 10.1038/nrm3011 21102611
23. Garofalo M. Condorelli G.L. Croce C.M. Condorelli G. 2010. MicroRNAs as regulators of death receptors signaling. Cell Death Differ. 17 (2): 200-208. 10.1038/cdd.2009.105 19644509
24. Garŕ C. Bianchi-Scarrá G. Sirito M. Musso M. Ravazzolo R. 1992. Lactoferrin binding sites and nuclear localization in K562(S) cells. J. Cell. Physiol. 153 (3): 477-482. 10.1002/jcp.1041530306 1447310
25. Gill G. 2005. Something about SUMO inhibits transcription. Curr. Opin. Genet. Dev. 15 (5): 536-541. 10.1016/j.gde.2005.07.004 16095902
26. Glozak M.A. Sengupta N. Zhang X. Seto E. 2005. Acetylation and deacetylation of non-histone proteins. Gene, 363: 15-23. 10.1016/j.gene.2005.09. 010 16289629
27. Goldberg G.S. Kunimoto T. Alexander D.B. Suenaga K. Ishidate F. Miyamoto K. et al. 2005. Full length and delta lactoferrin display differential cell localization dynamics, but do not act as tumor markers or significantly affect the expression of other genes. Med. Chem. 1 (1): 57-64. 10.2174/1573406053402532 16789886
28. Gupta R. Brunak S. 2002. Prediction of glycosylation across the human proteome and the correlation to protein function. Pac. Symp. Biocomput. 310-322. 11928486
29. Hames R.S. Wattam S.L. Yamano H. Bacchieri R. Fry A.M. 2001. APC/C-mediated destruction of the centrosomal kinase Nek2A occurs in early mitosis and depends upon a cyclin A-type D-box. EMBO J. 20 (24): 7117-7127. 10.1093/emboj/20.24.7117 11742988
30. Han I. Kudlow J.E. 1997. Reduced O glycosylation of Sp1 is associated with increased proteasome susceptibility. Mol. Cell. Biol. 17 (5): 2550-2558. 9111324
31. Hannoun Z. Greenhough S. Jaffray E. Hay R.T. Hay D.C. 2010. Post-translational modification by SUMO. Toxicology, 278 (3): 288-293. 10.1016/j.tox.2010.07.013 20674646
32. Hardivilĺ S. Hoedt E. Mariller C. Benaäraquo;ssa M. Pierce A. 2010. O-GlcNAcylation/phosphorylation cycling at Ser10 controls both transcriptional activity and stability of delta-lactoferrin. J. Biol. Chem. 285 (25): 19205-19218. 10.1074/jbc.M109.080572 20404350
33. Hart G.W. Haltiwanger R.S. Holt G.D. Kelly W.G. 1989. Glycosylation in the nucleus and cytoplasm. Annu. Rev. Biochem. 58 (1): 841-874. 10.1146/annurev.bi.58.070189.004205 2673024
34. He J. Furmanski P. 1995. Sequence specificity and transcriptional activation in the binding of lactoferrin to DNA. Nature, 373 (6516): 721-724. 10.1038/373721a0 7854459
35. Herman J.G. Baylin S.B. 2003. Gene silencing in cancer in association with promoter hypermethylation. N. Engl. J. Med. 349 (21): 2042-2054. 10.1056/NEJMra023075 14627790
36. Hoedt E. Hardivilĺ S. Mariller C. Elass E. Perraudin J.-P. Pierce A. 2010. Discrimination and evaluation of lactoferrin and delta-lactoferrin gene expression levels in cancer cells and under inflammatory stimuli using TaqMan real-time PCR. Biometals, 23 (3): 441-452. 10.1007/s10534-010-9305-5 20155437
37. Jans D.A. Briggs L.J. Gustin S.E. Jans P. Ford S. Young I.G. 1997. A functional bipartite nuclear localisation signal in the cytokine interleukin-5. FEBS Lett. 406 (3): 315-320. 10.1016/S0014-5793(97)00293-7 9136909
38. Johnson E.S. 2004. Protein modification by SUMO. Annu. Rev. Biochem. 73 (1): 355-382. 10.1146/annurev.biochem.73.011303.074118 15189146
39. Kamemura K. Hart G.W. 2003. Dynamic interplay between O-glycosylation and O-phosphorylation of nucleocytoplasmic proteins: a new paradigm for metabolic control of signal transduction and transcription. Prog. Nucleic Acid Res. Mol. Biol. 73: 107-136. 10.1016/S0079-6603(03)01004-3 12882516
40. Kim S.J. Yu D.Y. Pak K.W. Jeong S. Kim S.W. Lee K.K. 1998. Structure of the human lactoferrin gene and its chromosomal localization. Mol. Cells, 8 (6): 663-668. 9895117
41. Kirkin V. Dikic I. 2007. Role of ubiquitin-and Ubl-binding proteins in cell signaling. Curr. Opin. Cell Biol. 19 (2): 199-205. 10.1016/j.ceb.2007.02. 002 17303403
42. Kozak M. 2002. Pushing the limits of the scanning mechanism for initiation of translation. Gene, 299 (1-2): 1-34. 10.1016/S0378-1119(02)01056-9 12459250
43. Lahortiga I. Vázquez I. Agirre X. Larrayoz M.J. Vizmanos J.L. Gozzetti A. et al. 2004. Molecular heterogeneity in AML/MDS patients with 3q21q26 rearrangements. Genes Chromosomes Cancer, 40 (3): 179-189. 10.1002/gcc.20033 15138998
44. Lefebvre T. Dehennaut V. Guinez C. Olivier S. Drougat L. Mir A.-M. et al. 2010. Dysregulation of the nutrient/stress sensor O-GlcNAcylation is involved in the etiology of cardiovascular disorders, type-2 diabetes and Alzheimer's disease. Biochim. Biophys. Acta, 1800 (2): 67-79. 10.1016/j.bbagen.2009.08.008 19732809
45. Legrand D. Vigí K. Said E.A. Elass E. Masson M. Slomianny M.-C. et al. 2004. Surface nucleolin participates in both the binding and endocytosis of lactoferrin in target cells. Eur. J. Biochem. 271 (2): 303-317. 10.1046/j.1432-1033.2003.03929.x 14717698
46. Legrand D. Pierce A. Elass E. Carpentier M. Mariller C. Mazurier J. 2008. Lactoferrin structure and functions. Adv. Exp. Med. Biol. 606: 163-194. 10.1007/978-0-387-74087-4-6 18183929
47. Liao Y. Du X. Lönnerdal B. 2010. miR-214 regulates lactoferrin expression and pro-apoptotic function in mammary epithelial cells. J. Nutr. 140 (9): 1552-1556. 10.3945/jn.110.124289 20610637
48. Lin X. Liang M. Liang Y.-Y. Brunicardi F.C. Feng X.-H. 2003. SUMO-1/Ubc9 promotes nuclear accumulation and metabolic stability of tumor suppressor Smad4. J. Biol. Chem. 278 (33): 31043-31048. 10.1074/jbc.C300112200 12813045
49. Linder P. Lasko P.F. Ashburner M. Leroy P. Nielsen P.J. Nishi K. et al. 1989. Birth of the D-E-A-D box. Nature, 337 (6203): 121-122. 10.1038/337121a0 2563148
50. Liu D. Wang X. Zhang Z. Teng C.T. 2003. An intronic alternative promoter of the human lactoferrin gene is activated by Ets. Biochem. Biophys. Res. Commun. 301 (2): 472-479. 10.1016/S0006-291X(02)03077-2 12565886
51. Liu S.-W. Jiao X. Liu H. Gu M. Lima C.D. Kiledjian M. 2004. Functional analysis of mRNA scavenger decapping enzymes. RNA, 10 (9): 1412-1422. 10.1261/rna.7660804 15273322
52. Mann D.M. Romm E. Migliorini M. 1994. Delineation of the glycosaminoglycan-binding site in the human inflammatory response protein lactoferrin. J. Biol. Chem. 269 (38): 23661-23667. 8089135
53. Mariller C. Benaäraquo;ssa M. Hardivilĺ S. Breton M. Pradelle G. Mazurier J. Pierce A. 2007. Human delta-lactoferrin is a transcription factor that enhances Skp1 (S-phase kinase-associated protein) gene expression. FEBS J. 274 (8): 2038-2053. 10.1111/j.1742-4658.2007.05747.x 17371504
54. Mariller C. Hardivilĺ S. Hoedt E. Benaäraquo;ssa M. Mazurier J. Pierce A. 2009. Proteomic approach to the identification of novel delta-lactoferrin target genes: characterization of DcpS, an mRNA scavenger decapping enzyme. Biochimie, 91 (1): 109-122. 10.1016/j.biochi.2008.07.009 18725266
55. McCombs J.L. Teng C.T. Pentecost B.T. Magnuson V.L. Moore C.M. McGill J.R. 1988. Chromosomal localization of human lactotransferrin gene (LTF) by in situ hybridization. Cytogenet. Cell Genet. 47 (1-2): 16-17. 10.1159/000132496 3356163
56. McGrattan P. Logan A. Humphreys M. Bowers M. 2010. Jumping translocation in acute monocytic leukemia (M5b) with alternative breakpoint sites in the long arm of donor chromosome 3. Med. Oncol. 27 (3): 667-672. 10.1007/s12032-009-9266- 0 19629764
57. Melino G. Knight R.A. 2010. MicroRNAs meet cell death. Cell Death Differ. 17 (2): 189-190. 10.1038/cdd.2009.122 20062066
58. Morris D.R. Geballe A.P. 2000. Upstream open reading frames as regulators of mRNA translation. Mol. Cell. Biol. 20 (23): 8635-8642. 10.1128/MCB.20.23. 8635-8642.2000 11073965
59. Novoselov S.V. Kryukov G.V. Xu X.-M. Carlson B.A. Hatfield D.L. Gladyshev V.N. 2007. Selenoprotein H is a nucleolar thioredoxin-like protein with a unique expression pattern. J. Biol. Chem. 282 (16): 11960-11968. 10.1074/jbc.M701605200 17337453
60. Pan Y. Tsai C.-J. Ma B. Nussinov R. 2010. Mechanisms of transcription factor selectivity. Trends Genet. 26 (2): 75-83. 10.1016/j.tig.2009.12.003 20074831
61. Penco S. Pastorino S. Bianchi-Scarrà G. Garrè C. 1995. Lactoferrin down-modulates the activity of the granulocyte macrophage colony-stimulating factor promoter in interleukin-1β-stimulated cells. J. Biol. Chem. 270 (20): 12263-12268. 10.1074/jbc.270.20.12263 7744878
62. Penco S. Scarfi S. Giovine M. Damonte G. Millo E. Villaggio B. et al. 2001. Identification of an import signal for, and the nuclear localization of, human lactoferrin. Biotechnol. Appl. Biochem. 34 (3): 151-159. 10.1042/BA20010038 11730482
63. Pettersen E.F. Goddard T.D. Huang C.C. Couch G.S. Greenblatt D.M. Meng E.C. Ferrin T.E. 2004. UCSF Chimera'a visualization system for exploratory research and analysis. J. Comput. Chem. 25 (13): 1605-1612. 10.1002/jcc.20084 15264254
64. Rechsteiner M. Rogers S.W. 1996. PEST sequences and regulation by proteolysis. Trends Biochem. Sci. 21 (7): 267-271. 8755249
65. Rocchia W. Sridharan S. Nicholls A. Alexov E. Chiabrera A. Honig B. 2002. Rapid grid-based construction of the molecular surface and the use of induced surface charge to calculate reaction field energies: applications to the molecular systems and geometric objects. J. Comput. Chem. 23 (1): 128-137. 10.1002/jcc.1161 11913378
66. Rogers S. Wells R. Rechsteiner M. 1986. Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science, 234 (4774): 364-368. 10.1126/science.2876518 2876518
67. Sadoul K. Boyault C. Pabion M. Khochbin S. 2008. Regulation of protein turnover by acetyltransferases and deacetylases. Biochimie, 90 (2): 306-312. 10.1016/j.biochi.2007.06.009 17681659
68. Sanner M.F. Olson A.J. Spehner J.C. 1996. Reduced surface: an efficient way to compute molecular surfaces. Biopolymers, 38 (3): 305-320. 10.1002/(SICI)1097-0282(199603)38:3<305::AID-BIP4>3.0.CO;2-Y 8906967
69. Shen V. Liu H. Liu S.-W. Jiao X. Kiledjian M. 2008. DcpS scavenger decapping enzyme can modulate pre-mRNA splicing. RNA, 14 (6): 1132-1142. 10.1261/rna.1008208 18426921
70. Siebert P.D. Huang B.C. 1997. 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 (6): 2198-2203. 10.1073/pnas.94.6.2198 9122171
71. Son K.-N. Park J. Chung C.-K. Chung D.K. Yu D.-Y. Lee K.-K. Kim J. 2002. Human lactoferrin activates transcription of IL-1β gene in mammalian cells. Biochem. Biophys. Res. Commun. 290 (1): 236-241. 10.1006/bbrc.2001.6181 11779159
72. Teng C.T. Beard C. Gladwell W. 2002. Differential expression and estrogen response of lactoferrin gene in the female reproductive tract of mouse, rat, and hamster. Biol. Reprod. 67 (5): 1439-1449. 10.1095/biolreprod.101.002089 12390874
73. Teng C. Gladwell W. Raphiou I. Liu E. 2004. Methylation and expression of the lactoferrin gene in human tissues and cancer cells. Biometals, 17 (3): 317-323. 10.1023/B:BIOM.0000027711.13818.8a 15222484
74. Testoni N. Borsaru G. Martinelli G. Carboni C. Ruggeri D. Ottaviani E. et al. 1999. 3q21 and 3q26 cytogenetic abnormalities in acute myeloblastic leukemia: biological and clinical features. Haematologica, 84 (8): 690-694. 10457403
75. Tsvetkov L.M. Yeh K.-H. Lee S.-J. Sun H. Zhang H. 1999. p27(Kip1) ubiquitination and degradation is regulated by the SCF(Skp2) complex through phosphorylated Thr187 in p27. Curr. Biol. 9 (12): 661-664. 10.1016/S0960- 9822(99)80290-5 10375532
76. van Berkel P.H. Geerts M.E. van Veen H.A. Mericskay M. de Boer H.A. Nuijens J.H. 1997. N-terminal stretch Arg2, Arg3, Arg4 and Arg5 of human lactoferrin is essential for binding to heparin, bacterial lipopolysaccharide, human lysozyme and DNA. Biochem. J. 328 (1): 145-151. 9359845
77. Verger A. Perdomo J. Crossley M. 2003. Modification with SUMO. A role in transcriptional regulation. EMBO Rep. 4 (2): 137-142. 10.1038/sj.embor.embor738 12612601
78. Ward P.P. Paz E. Conneely O.M. 2005. Multifunctional roles of lactoferrin: a critical overview. Cell. Mol. Life Sci. 62 (22): 2540-2548. 10.1007/s00018-005-5369-8 16261256
79. Yang X.-J. Seto E. 2008. Lysine acetylation: codified crosstalk with other posttranslational modifications. Mol. Cell, 31 (4): 449-461. 10.1016/j.molcel.2008.07.002 18722172
80. Yang X. Su K. Roos M.D. Chang Q. Paterson A.J. Kudlow J.E. 2001. O-linkage of N-acetylglucosamine to Sp1 activation domain inhibits its transcriptional capability. Proc. Natl. Acad. Sci. U.S.A. 98 (12): 6611-6616. 10.1073/pnas.111099998 11371615
81. Yang W.H. Kim J.E. Nam H.W. Ju J.W. Kim H.S. Kim Y.S. Cho J.W. 2006. Modification of p53 with O-linked N-acetylglucosamine regulates p53 activity and stability. Nat. Cell Biol. 8 (10): 1074-1083. 10.1038/ncb1470 16964247
82. Zhang H. Kobayashi R. Galaktionov K. Beach D. 1995. p19Skp1 and p45Skp2 are essential elements of the cyclin A-CDK2 S phase kinase. Cell, 82 (6): 915-925. 10.1016/0092-8674(95)90271-6 7553852