The vitamin D receptor-mediated activation of phosphatidylinositol 3-kinase (PI3Kα) plays a role in the 1α,25-dihydroxyvitamin D 3-stimulated increase in steroid sulphatase activity in myeloid leukaemic cell lines

Journal of Cellular Biochemistry

Volumn 103, Issue 5, 2008, Pages 1551-1572

  Hughes, Philip J ^a   Lee, Jimmy S ^b,c   Reiner, Neil E ^b,c   Brown, Geoffrey ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c VANCOUVER COASTAL HEALTH RESEARCH INSTITUTE   (Canada)

Author keywords

Genomic and non genomic signalling; Myeloid cells; Phosphatidylinositol 3 kinase; Steroid sulphatase; Vitamin D receptor

Indexed keywords

1,3,24 TRIHYDROXY 26,27 CYCLO 9,10 SECOCHOLESTA 5,7,10(19),22 TETRAENE 25 CARBOXYLIC ACID BUTYL ESTER; 2 MORPHOLINO 8 PHENYLCHROMONE; CALCITRIOL; PHOSPHATIDYLINOSITOL 3 KINASE; PX 866; STERYL SULFATASE; UNCLASSIFIED DRUG; VITAMIN D DERIVATIVE; VITAMIN D RECEPTOR; WORTMANNIN; ZK 168281;

ARTICLE; CANCER CELL CULTURE; CONTROLLED STUDY; DRUG INHIBITION; ENZYME ACTIVATION; ENZYME ACTIVITY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MYELOID LEUKEMIA; PRIORITY JOURNAL;

1-PHOSPHATIDYLINOSITOL 3-KINASE; CALCITRIOL; ENZYME INDUCTION; HL-60 CELLS; HUMANS; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, CALCITRIOL; SIGNAL TRANSDUCTION; STERYL-SULFATASE; U937 CELLS; VITAMINS;

EID: 41749105769     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.21545     Document Type: Article

References (99)

1. Ai Z, Misra S, Susa M, Variticovski L, Cohen C. 1995. Phosphatidylinositol 3-kinase activity in murine erythroleukemia cells during DMSO-induced differentiation. Exp Cell Res 219:454-460.
2. Baron S, Mamin M, Beaudoin C, Leotoing L, Communal L, Veyssiere G, Morel L. 2004. Androgen receptor mediates non-genomic activation of phosphatidylinositol 3-OH kinase in androgen-sensitive epithelial cells. J Biol Chem 279:14579-14586.
3. Barsony J, Prufer K. 2002. Vitamin D receptor and retinoid X receptor interactions in motion. Vitam Horm 65:345-376.
4. 3 stimulates phosphorylation of IκBα and synergises with TPA to induce nuclear translocation of NF-κB during monocytic differentiation of NB4 leukaemia cells. Exp Cell Res 272:176-184.
5. Bertagnolo V, Brugnoli F, Marchiso M, Capitano S. 2004. Inositide-modifying enzymes: A cooperative role in regulating nuclear morphology during differentiation of myeloid cells. J Biol Regul Homeost Agents 18:381-386.
6. 2-vitamin
7. Bortul R, Tazzari P, Cappellini A, Tabellini G, Billi A, Bareggi R, Manzoli L, Cocco L, Martelli A. 2003. Constitutively active Akt1 protects HL60 leukaemia cells from TRAIL-induced apoptosis through a mechanism involving NF-κB activation and cFLIP(L) up-regulation. Leukaemia 17:379-389.
8. 3 correlates with tyrosine phosphorylation of the vitamin D receptor (VDR) and VDR-Src interaction. J Cell Biochem 79:274-281.
9. S6K cascade through phosphatidylinositol 3-kinase in human blasts. Mol Endocrinol 19:102-112.
10. 3 induces translocation of the vitamin D receptor (VDR) to the plasma membrane in skeletal muscle cells. J Cell Biochem 86:128-135.
11. Castillo A, Sanchez-Martinez R, Jimenez-Lara A, Steinmeyer A, Zugel U, Aranda A. 2006. Characterization of vitamin D receptor ligands with cell-specific and dissociated activity. Mol Endocrinol 20:3093-3104.
12. Cataldi A, Di Pietri R, Centurione L, Grilli A, Miscia S. Phosphatidylinosotol 3-kinase activation and atypical protein kinase Cζ phosphorylation characterise the DMSO signalling in erythroleukaemia cells. Cell Signal 2000. 12:667-672.
13. Chang H, Oh P, Ingber D, Huang S. 2006. Multistage and multistep dynamics in neutrophil differentiation. BMC Cell Biol 7:11.
14. Chaussade C, Rewcastle G, Kendall J, Denny W, Cho K, Gronning L, Chong M, Anagnostou S, Jackson S, Daniele N, Sheperd P. 2007. Evidence for functional redundancy in class-IA PI3-kinase isoforms in insulin signalling. Biochem J 404:449-458.
15. Chong Y, Colston K, Jiang W, Sharma A, Mokbel K. 2006. The relationship between the insulin-like growth factor-1 system and the oestrogen metabolising enzymes in breast cancer tissue and its adjacent non-cancerous tissue. Breast Cancer Res Treat 99:275-288.
16. Condliffe A, Davidson K, Anderson K, Ellson C, Crabbe T, Okkenhaug K, Vanhaesebroeck B, Turner M, Webb L, Wymann M, Hirsch E, Ruckle T, Camps M, Rommel C, Jackson S, Chilvers E, Stephens L, Hawkins P. 2005. Sequential activation of class 1B and class 1A PI3K is important for the primed respiratory burst of human but not murine neutrophils. Blood 106:1432-1440.
17. Cosemans J, Munnix I, Wetzker R, Heller R, Jackson S, Heemskerk J. 2006. Continuous signalling via PI3K isoforms β and γ is required for platelet ADP receptor function in dynamic thrombus stabilization. Blood 108:3045-3052.
18. Dhandapani K, Wade F, Wakade C, Mahesh V, Brann D. 2005. Neuroprotection by stem cell factor in rat cortical neurones involved AKT and NF-κB. J Neurochem 95:9-19.
19. Foukas L, Daniele N, Ktori C, Anderson K, Jensen J, Shepherd P. 2002. Direct effect of caffeine and theophylline on p110δ and other phosphoinositde 3-kinases. J Biol Chem 277:37124-37130.
20. Foukas L, Claret M, Pearce W, Okkenhaug K, Meek S, Peskett E, Sancho S, Smith A, Withers J, Vanhaesebroeck B. 2006. Critical role for the p110α phosphoinositide-3-OH kinase in growth and metabolic regulation. Nature 441:366-370.
21. Furuya F, Hanover J, Cheng S. 2006. Activation of the phosphatidylinositol 3-kinase signaling by a mutant throid hormone β receptor. Proc Natl Acad Sci USA 103:1780-1785.
22. Furuya F, Guigon C, Zhao L, Lu C, Hanover J, Cheng S. 2007. Nuclear receptor co-repressor (NcoR) is a novel regulator of PI3K signalling. Mol Cell Biol DOI: 10.1128/MCB.00900-07.
23. Gareus R, Huth M, Breiden B, Nenci A, Rosch N, Haasw I, Bloch W, Sandhoff K, Pasparakis M. 2007. Normal epidermal differentiation but impaired skin-barrier formation upon keratinocyte-restricted IKK1 ablation. Nat Cell Biol 9:461-466.
24. Gillooly D, Melendez A, Hockaday A, Harnett M, Allen J. 1999. Endoxytosis and vesicular trafficking of immune complexes and activation of phospholipase D by the human high affinity IgG receptor requires distinct phosphoinositides 3-kinase activities. Biochem J 344:605-611.
25. Gocek E, Kielbinski M, Marcinkowska E. 2007. Activation of intracellular signalling pathways is necessary for an increase in VDR expression and its nuclear translocation. FEBS Lett 581:1751-1757.
26. Gomez-Mouton C, Lacalle R, Mira E, Jiminez-Baranda S, Barber D, Carrera A, Martinez A, Manes S. 2004. Dynamic redistribution of raft domains as an organizing platform for signalling during cell chemotaxis. J Cell Biol 164:759-768.
27. Greger J, Fursov N, Cooch N, McLarney S, Freedman L, Edwards D, Cheskis B. 2007. Phosphorylation of MNAR promotes estrogen activation of PI3 kinase. Mol Cell Biol 27:1904-1913.
28. Guzman M, Neering S, Upchurch D, Grimes B, Howard D, Rizzieri D, Luger S, Jordan C. 2001. Nuclear factor-κB is constitutively activated in primitive human acute myelogenous leukaemia cells. Blood 98:2301-2307.
29. Hawkins P, Anderson K, Davidson K, Stephens L. 2006. Signalling through Class I PI3Ks in mammalian cells. Biochem Soc Trans 34:647-662.
30. Hayakawa M, Kaizawa H, Moritomo H, Koizumi T, Ohishi T, Okada M, Ohta M, Tsukamoto S, Parker P, Workman P, Waterfield M. 2006. Synthesis and biological evaluation of 4-morpholino-2-phenylquinazolines and related derivatives as novel PI3 kinas e p110α inhibitors. Bioorg Med Chem 14:6847-6858.
31. Hehner S, Hofmann T, Droge W, Schmitz M. 1999. The anti-inflammatory seaquiterpene lactone parthenolide inhibits NF-κB by targeting the IκB kinase complex. J Immunol 163:5617-5623.
32. 3 is mediated by a lack of ligand induced vitamin D interaction with coactivators. J Biol Chem 275:16506-16512.
33. Hiromura M, Okada F, Obata T, Auguin D, Shibata T, Roumestand C, Noguchi M. 2004. Inhibition of Akt kinase activity by a peptide spanning the βA strand of the proto-oncogene T CL1. J Biol Chem 279:53407-53418.
34. 3-phosphoinositide 3-kinase pathway. J Cell Sci 117:2131-2140.
35. Hu Y, Qiao L, Wang S, Rong S, Meuillet E, Berggren M, Gallegos A, Powis G, Kozikowski A. 2000. 3-(Hydroxymethyl)-bearing phosphatidylinositol ether lipid analogues and carbonate surrogates block PI3-K, Akt and cancer cell growth. J Med Chem 43:3045-3051.
36. nuc-mediated activation of the RAS/RAF/ERK-MAP kinase signalling pathway. J Cell Biochem 98:590-617.
37. 3-induced differentiation of HL60 cells. Biochem J 355:361-371.
38. 3 stimulates steroid sulfatase activity via a nuclear receptor in acute myeloid leukaemia cell lines but via a membrane receptor in NB4 acute promyelocytic leukaemia cell lines. J Cell Biochem 94:1175-1189.
39. 3 in vivo and in vitro. Mol Endocrinol 18:2660-2671.
40. Ihle N, Paine-Murrieta G, Berggren M, Baker A, Tate W, Wipf P, Abraham R, Kirkpatrick D, Powis G. 2005. The phosphatidylinositol 3-kinase inhibitor PX-866 overcomes resistance to the epidermal growth factor receptor inhibitor gefintib in A-549 human non-small cell lung cancer xenografts. Mol Caner Ther 4:1349-1357.
41. Jackson S, Scoenwaelder S, Goncalves I, Nesbitt W, Yan C, Wright C, Kenche V, Anderson K, Dopheide S, Yuan Y, Sturgeon S, Prabaharan H, Thompson P, Smith G, Sheperd P, Daniele N, Kulkarni S, Abbott B, Saylik D, Jones C, Lu L, Guiliano S, Hughan S, Angus J, Robertson A, Salem H. 2005. PI 3-kinase p110β: A new target for anti-thrombotic therapy. Nat Med 11:507-514.
42. 2)-induced apoptosis in lymhocytes by reciprocal NF-κB activation and p53 inhibition via PI3K-dependent pathway. Growth Factors 24:67-78.
43. Jones G, Strugnell S, DeLuca H. 1998. Current understanding of the molecular actions of vitamin D. Physiol Rev 78:1193-1231.
44. Keifer J, Guttridge D, Ashburner B, Baldwin A. 2001. Inhibition of NF-κB activity by thalidomide through suppression of IκB kinase activity. J Biol Chem 276:22382-22387.
45. 3-MARRS receptor: Multiple functional roles in diverse cell systems. Curr Med Chem 14:1087-1093.
46. 3-occupied vitamin D receptors with cellular membrane acceptance sites. Endocrinol 137:3649-3658.
47. Kim S, Kanno A, Ozawa T, Tao H, Umezawa Y. 2007. Non-genomic activity of ligands in the association of androgen receptor with Src. ACS Chem Biol DOI: 10.1021/cb7000439.
48. Kitawaki J. 2006. Adenomyosis: The pathophysiology of an oestrogen-dependent disease. Best Pract Res Clin Obstet Gynaecol 20:493-502.
49. Kivineva M, Blauer M, Syvala H, Tammela T, Tuohimaa P. 1998. localization of 1,25-dihydroxyvitamin D3 receptor (VDR) expression in human prostate. J Ster Biochem Mol Biol 66:121-127.
50. Klopot A, Hance K, Peleg S, Barsony J, Fleet J. 2006. Nucleocytoplasmic cycling of the vitamin D receptor in the enterocyte-like cell line, Caco-2. J Cell Biochem 100:6127-6628.
51. Kobari M, Yang Z, Gong D, Heissmeyer V, Zhu H, Jung Y, Gakidis M, Rao A, Sekine T, Ikegami F, Yuan C, Yuan J. 2004. Wedelolactone suppresses LPS-induced caspase-11 expression by directly inhibiting the IKK complex. Cell Death Differ 11:123-130.
52. Kozikowski A, Sun H, Brognard J, Dennis P. 2003. Novel PI analogues selectively block activation of the pro-survival serine, threonine kinase Akt. J Am Chem Sci 125:1144-1145.
53. Le Mellay V, Lasmoles F, Lieberherr M. 1999. Gα(q/11) and Gβγ proteins and membrane signalling of calcitrol and estradiol. J Cell Biochem 75:138-146.
54. Lee J, Hmama Z, Mui A, Reiner N. 2004. Stable gene silencing in human monocytic cell lines using lentiviral-delivered siRNA: Silencing of the p110α isoform of phosphoinositide 3-kinase reveals differential regulation of adherence induced by 1α,25-dihydroxyvitamin D3 and bacterial lipopolysaccharide. J Biol Chem 279:9379-9388.
55. Lee Y, Shim H, Yu H, Song E, Park J, Kwon K, Parl J, Rho H, Park B, Han M, Kim J. 2005. Dimethylsulphoxide induces expression of the tumour suppressor protein PTEN through nuclear factor-κB activation in HL60 cells. Leuk Res 29:401-405.
56. Lin YZ, Veach R, Togerson T, Hawiger J. 1995. Inhibition of nuclear translocation of transcription factor NF-κB by a synthetic peptide containing a cell membrane-permeable motif and nuclear localization sequence. J Biol Chem 270:14255-14258.
57. Liu Q, Ning W, Dantzer R, Freund G, Kelley K. 1998. Activation of protein kinase C-ζ and phosphatidylinositol 3′-kinase and promotion of macrophage differentiation by insulin-like growth factor-1. J Immunol 160:1393-1401.
58. Lord J, Bunce C, Duncan R, Phillips I, Shennan K, Docherty K, Brown G. 1988. Changes in insulin receptor expression in HL60 cells induced to differentiate towards neutrophils and monocytes. J Mol Endocrinol 1:197-201.
59. Manning B, Cantley L. 2007. AKT/PKB signalling: Navigating downstream. Cell 129:1261-1274.
60. Martelli A, Nyakern M, Tabellini G, Bortul R, Tazzari P, Evangelisti C, Cocco L. 2006. Phosphoinositide 3-kinase/Akt signalling pathway and its therapeutic implications for human acute myeloid leukaemia. Leukaemia 20:911-928.
61. Masiá S, Alvarez S, De Lera A, Darettino D. 2007. Rapid, non-genomic actions of retinoic acid on phosphatidylinositol-3-kinase signalling pathway mediated by the retinoic acid receptor. Mol Endocrinol DOI: 10.1210/me.2007-0062.
62. Matkovic K, Brugnoli F, Bertagnolo V, Banfic H, Visnjic D. 2006. The role of the nuclear Akt activation and Akt inhibitors in all-trans-retinoic acid-differentiated HL-60 cells. Leukemia 20:941-951.
63. Melendez A, Harnett M, Allen J. 1999. FcgRI activation of phospholipase Cγ1 and protein kinase C in dibutyrl cAMP-differentiated U937 cells is dependent solely on the tyrosine-kinase activated form of phosphatidylinositol- 3-kinase. Immunology 98:1-8.
64. Monks N, Pardee A. 2006. Targeting the NF-κB pathway in estrogen receptor negative MDA-MB-231 breast cancer cells using small inhibitory RNAs. J Cell Biochem 98:221-233.
65. Nakshatri H, Bhat-Nakshatri P, Martin D, Goulet R, Sledge G. 1997. Constitutive activation of NF-κB during progression of breast cancer to hormone-independent growth. Mol Cell Biol 17:3629-3639.
66. Ng J, Nesaretham K, Reimann K, Lai L. 2000. Effect of retinoic acid and palm oil carotenoids on oestrone sulfatase and oestradiol-17β- hydroxysteroid dehydrogenase activities in MCF-7 and MDA-MB-231 breast cancer cell lines. Int J Cancer 88:135-138.
67. Norman A. 2006. Vitamin D receptor (VDR): New assignments for an already busy receptor. Endocrinology 147:5448-5542.
68. Norman A, Mizwicki M, Norman D. 2004. Steroid hormone rapid actions, membrane receptors and a conformation ensemble model. Nat Rev Drug Discov 3:27-41.
69. 3-23,26- lactone depends on the primary structure of the carboxyterminal region of the vitamin D receptor. Mol Endocrinol 19:1147-1157.
70. Ozes O, Mayo L, Gustin J, Pfeiffer S, Pfeiffer L, Donner D. 1999. NF-κB activation by tumour necrosis factor requires Akt serine-threonine kinase. Nature 401:82-85.
71. Perez-Tenorio G, Alkhor L, Olsson B, Waltersson M, Nordenskjold B, Rutqvist L, Skoog L, Stal O. 2007. PIK3CA mutations and PTEN loss correlate with similar prognostic factors and are not mutually exclusive in breast cancer. Clin Canc Res 13:3577-3584.
72. Pomel V, Klicic J, Covini D, Church D, Shaw J, Troulin K, Burgat-Charvillon F, Valognes D, Camps M, Chabert C, Gillieron C, Francon B, Perrin D, Leroy D, Gretener D, Nichols A, Vitte P, Carboni S, Rommel C, Schwarz M, Ruckle T. 2006. Furan-2-ylmethylene thiazolidinediones as novel, potent, and selective inhibitors of phosphoinositide 3-kinase γ. J Med Chem 49:3857-3871.
73. Purohit A, Reed M. 1992. Oestreogen sulfatase activity in hormone-dependent and hormone-independent breast cancer cells: Modulation by steroidal and non-steroidal therapeutic agents. Int J Cancer 50:901-905.
74. Reed M, Purohit A, Woo L, Newman S, Potter B. 2005. Steroid sulfatase: Molecular biology, regulation, and inhibition. Endocr Rev 26:171-202.
75. Sasano H, Suzuki T, Nakate T, Moriya T. 2006. New development in intracrinology of breast cancer. Breast cancer 13:129-136.
76. Selcer K, Hedge P, Li P-K. 1997. Inhibition of estrone sulfatase and proliferation of human breast cancer cells by non-steroidal ( p-O-sulfamoyl)-N-alkanoyl tyramines. Cancer Res 57:702-707.
77. Selcer K, DiFrancesca H, Chandra A, Li P-K. 2007. Immunohistochemical analysis of steroid sulfatase in human tissues. J Ster Biochem Mol Biol DOI: 10.1016/j.jsbmb.2006.12.105.
78. Seveau S, Eddy R, Maxfield F, Pierini M. 2001. Cytoskeleton-dependent membrane domain segregation during neutrophil polarization. Mol Biol Cell 12:3550-3562.
79. Simoncini T, Hafezi-Moghadam A, Brazil D, Ley K, Chin W, Liao J. 2000. Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol 3-kinase. Nature 407:538-541.
80. Sliva D, Rizzo M, English D. 2002. Phosphatditylinositol 3-kinase and NF-κB regulate motility of invasive MDA-MB-231 human breast cancer cells by secretion of the urokinase-type plasminogen activator. J Biol Chem 277:3150-3157.
81. 3-induced monocyte antimycobacterial activity is regulated by phosphatidylinositol 3-kinase and mediated by the NADPH-dependent phagocyte oxidase. J Biol Chem 276:35482-35493.
82. Smuc T, Rupreht R, Šinkovec J, Adamski J, Rižner T. 2005. Expression analysis of estrogen-metabolizing enzymes in human endometrial cancer. Mol Cell Endocrinol 248:114-117.
83. Songyang Z, Shoelson S, Chaudhuri M, Gish G, Pawson T, Haser W, King F, Roberts T, Ratnofsky S, Lechleider R, Neel B, Birge R, Fajardo E, Chou M, Hanafusa H, Schaffhausen B, Cantley L. 1993. SH2 domains recognize specific phosphopeptide sequences. Cell 72:767-778.
84. Stanway S, Purohit A, Woo L, Sufi S, Vigushin D, Ward R, Wilson R, Stanczyk F, Dobbs N, Kulinskaya E, Elliott M, Potter B, Reed M, Coombes R. 2006. Phase I study of STX 64 (667 coumate) in breast cancer patients: The first study of a steroid sulfatase inhibitor. Clin Cancer Res 12:1585-1592.
85. Sun M, Yang L, Feldman R, Sun X-M, Bhalla K, Jove R, Nicosia S, Cheng J. 2003. Activation of phosphatidylinositol 3-kinase/Akt pathway by androgen through interaction of p85α, androgen receptor and Src. J Biol Chem 278:42992-43000.
86. Suzuki T, Miki Y, Nakamura Y, Moriya T, Ito K, Ohuchi N, Sasano H. 2005. Sex steroid-producing enzymes in human breast cancer. Endocrine-related Cancer 12:701-720.
87. Tanaka K, Kubushiro K, Iwamori Y, Okiri Y, Kiguchi K, Ishiwata I, Tsukazaki K, Nozawa S, Iwamori M. 2003. Estrogen sulfotransferase and sulphatase: Roles in the regulation of estrogen activity in human uterine endometrial carciniomas. Canc Sci 94:871-876.
88. 3 induces biphasic NF-κB responses during HL-60 leukaemia cells differentiation through protein induction and PI3K/Akt-dependent phosphorylation/ degradation of IκB. Exp Cell Res 313:1722-1739.
89. Tsunoda Y, Shimizu Y, Tsunoda A, Takimoto M, Sakamoto M, Kusano M. 2006. Steroid sulfatase in breast carcinoma and change in serum estrogen levels after operation. Acta Oncol 45:584-589.
90. Upadhyay A, Singh S, Chhipa R, Vijayakumar M, Ajay A, Bhat M. 2006. Methyl-β-cyclodextrin enhances the susceptibility of human breast cancer cells to carboplatin and 5-fluorouracil: Involvement of Akt, NF-κB and Bcl-2 toxicol. Appl Pharmacol 216:177-185.
91. Utsunomiya H, Ito K, Suzuki T, Kitamura T, Kaneko C, Nakata T, Niikura H, Okamura K, Yaegashi N, Sasano H. 2004. Steroid sulfatase and estrogen sulfotransferase in human endometrial carcinoma. Clin Cancer Res 10:5850-5856.
92. 3 and Cdc42 augment RhoA activity at the back as well as signals at the front. J Cell Biol 174:437-445.
93. 3 and analogs through the ligand binding domain of the vitamin D receptor in osteoblasts and osteocytes. Mediation by Src, phosphatidylinositol 3- and JNK kinases. J Biol Chem 280:14130-14137.
94. 3 target genes. Mol Endocrinol 19:2685-2695.
95. Wu-Wong R, Nakane M, Ma J, Dixon D, Gagne G. 2006. Vitamin D receptor (VDR) localization in human promyelocytic leukaemia cells. Leuk Lymphoma 47:727-732.
96. Yanaihara A, Otsuka Y, Iwasaki S, Okai T, Yanaihara T. 2005. Strong expression of steroid sulfatase in human cumulus cells in patients with endometriosis. Fertil Steril 84:465-467.
97. Ye B, Akamatsu M, Shoelson S, Wolf G, Giorgetti-Peraldi S, Yan X, Roller P, Burke T. 1995. L-O-(2-malonyl)tyrosine: A new phosphotyrosyl mimetic for the preparation of Src homology 2 domain inhibitory peptides. J Med Chem 28:4270-4275.
98. 3 and participates in its anti-apoptotic effect and cell cycle control in differentiating HL60 cells. Cell Cycle 5:447-451.
99. Zhou Y, Eppenberger-Castori S, Marx C, Yau C, Scott G, Eppenberger U, Benz C. 2005. Activation of nuclear factor-κB (NFκB) identifies a high-risk subset of hormone dependent breast cancers. Int J Biochem Cell Biol 37:1130-1144.