Skip to main content
SpringerLink
Log in

Granulocytic differentiation of HL-60 promyelocytic leukemia cells is associated with increased expression of Cul5

  • Published:
In Vitro Cellular & Developmental Biology - Animal Aims and scope Submit manuscript

Abstract

The human HL-60 promyelocytic leukemia cell line has been widely used as a model for studying granulocytic differentiation. All-trans retinoic acid (ATRA) treatment of HL-60 cells promotes granulocytic differentiation and is effective as differentiation therapy for patients with acute promyelocytic leukemia. The identification of genes that are transcriptionally regulated by ATRA has provided insight into granulocytic differentiation and differentiation therapy. The Asb-2 (ankyrin repeat SOCS box 2) gene has previously been identified as a transcriptional target in ATRA-treated HL-60 cells. The ASB-2 protein forms an E3 ubiquitin ligase complex with the proteins, Cul5, regulator of cullin 2 (ROC2), and elongin B and C. The purpose of this study was to determine if there is increased expression of Cul5 during granulocytic differentiation of HL-60 cells. To induce granulocytic differentiation, HL-60 cells were treated for 5 d with ATRA and differentiation was confirmed by examining superoxide anion production, nuclear morphology, and changes in the expression of CD11b, CD13, and CD15. Quantitative real-time RT-PCR was used to measure Cul5 mRNA expression and also the expression of other components of the E3 ubiquitin ligase (ASB-2, ROC2, elongin B and C). Granulocytic differentiation of HL-60 cells was associated with a 1.6-, 1.7-, and 23-fold statistically significant (P ≤ 0.05) increase in mRNA expression for Cul5, ROC2, and ASB-2, respectively. No significant change was found in elongin B and C mRNA expression. Using Western blot analysis, the expression of Cul5 protein was increased 6.5-fold with granulocytic differentiation of the HL-60 cells. Increased expression of multiple components of the Cul5-containing E3 ubiquitin ligase complex with ATRA treatment of HL-60 cells indicates that this complex may play an important role in granulocytic differentiation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5.
Figure 6.

Similar content being viewed by others

References

  • Aso, T.; Lane, W. S.; Conaway, J. W.; Conaway, R. C. Elongin (SIII): a multisubunit regulator of elongation by RNA polymerase II. Science. 269: 1439–1443; 1995. doi:10.1126/science.7660129.

    Article  PubMed  CAS  Google Scholar 

  • Ayyub, C.; Sen, A.; Gonsalves, F.; Badrinath, K.; Bhandari, P.; Shashidhara, L. S.; Krishna, S.; Rodrigues, V. Cullin-5 plays multiple roles in cell fate specification and synapse formation during Drosophila Development. Dev. Dyn. 232: 865–875; 2005. doi:10.1002/dvdy.20322.

    Article  PubMed  CAS  Google Scholar 

  • Birnie, G. D. The HL60 cell line: a model system for studying human myeloid cell differentiation. Br. J. Cancer Suppl. 9: 41–45; 1988.

    PubMed  CAS  Google Scholar 

  • Brackman, D.; Lund-Johansen, F.; Aarskog, D. Expression of cell surface antigens during the differentiation of HL-60 cells induced by 1,25-dihydroxyvitamin D3, retinoic acid and DMSO. Leuk. Res. 19: 57–64; 1995. doi:10.1016/0145-2126(94)00061-E.

    Article  PubMed  CAS  Google Scholar 

  • Bradsher, J. N.; Jackson, K. W.; Conaway, R. C.; Conaway, J. W. RNA polymerase II transcription factor SIII. I. Identification, purification, and properties. J. Biol. Chem. 268: 25587–25593; 1993a.

    PubMed  CAS  Google Scholar 

  • Bradsher, J. N.; Tan, S.; McLaury, H. J.; Conaway, J. W.; Conaway, R. C. RNA polymerase II transcription factor SIII. II. Functional properties and role in RNA chain elongation. J. Biol. Chem. 268: 25594–25603; 1993b.

    PubMed  CAS  Google Scholar 

  • Breitman, T. R.; Selonick, S. E.; Collins, S. J. Induction of differentiation of the human promyelocytic leukemia cell line (HL-60) by retinoic acid. Proc. Natl. Acad. Sci. U.S.A. 77: 2936–2940; 1980. doi:10.1073/pnas.77.5.2936.

    Article  PubMed  CAS  Google Scholar 

  • Burnatowska-Hledin, M. A.; Kossoris, J. B.; Van Dort, C. J.; Shearer, R. L.; Zhao, P.; Murrey, D. A.; Abbott, J. L.; Kan, C. E.; Barney, C. C. T47D breast cancer cell growth is inhibited by expression of VACM-1, a cul-5 gene. Biochem. Biophys. Res. Commun. 319: 817–825; 2004. doi:10.1016/j.bbrc.2004.05.057.

    Article  PubMed  CAS  Google Scholar 

  • Burnatowska-Hledin, M. A.; Spielman, W. S.; Smith, W. L.; Shi, P.; Meyer, J. M.; Dewitt, D. L. Expression cloning of an AVP-activated, calcium-mobilizing receptor from rabbit kidney medulla. Am. J. Physiol. 268: F1198–F1210; 1995.

    PubMed  CAS  Google Scholar 

  • Byrd, P. J.; Stankovic, T.; McConville, C. M.; Smith, A. D.; Cooper, P. R.; Taylor, A. M. Identification and analysis of expression of human VACM-1, a cullin gene family member located on chromosome 11q22-23. Genome. Res. 7: 71–75; 1997. doi:10.1101/gr.7.1.71.

    Article  PubMed  CAS  Google Scholar 

  • Carter, S. L.; Negrini, M.; Baffa, R.; Gillum, D. R.; Rosenberg, A. L.; Schwartz, G. F.; Croce, C. M. Loss of heterozygosity at 11q22-q23 in breast cancer. Cancer Res. 54: 6270–6274; 1994.

    PubMed  CAS  Google Scholar 

  • Castaigne, S.; Chomienne, C.; Daniel, M. T.; Ballerini, P.; Berger, R.; Fenaux, P.; Degos, L. All-trans retinoic acid as a differentiation therapy for acute promyelocytic leukemia. I. Clinical results. Blood. 76: 1704–1709; 1990.

    PubMed  CAS  Google Scholar 

  • Ceremuga, T. E.; Yoa, X. L.; Alam, H. B.; McCabe, J. T. Alterations of Cullin-5 mRNA levels in the rat central nervous system following hemorrhagic shock. Neurol. Res. 25: 211–216; 2003a. doi:10.1179/016164103101201229.

    Article  PubMed  CAS  Google Scholar 

  • Ceremuga, T. E.; Yao, X. L.; Xia, Y.; Mukherjee, D.; McCabe, J. T. Osmotic stress increases Cullin 5 (cul-5) mRNA in the rat cerebral cortex, hypothalamus and kidney. Neurosci. Res. 45: 305–311; 2003b. doi:10.1016/S0168-0102(02)00228-6.

    Article  PubMed  CAS  Google Scholar 

  • Chomczynski, P.; Sacchi, N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162: 156–159; 1987. doi:10.1016/0003-2697(87)90021-2.

    Article  PubMed  CAS  Google Scholar 

  • Collins, S. J. The HL-60 promyelocytic leukemia cell line: Proliferation, differentiation, and cellular oncogene expression. Blood. 70: 1233–1244; 1987.

    PubMed  CAS  Google Scholar 

  • Collins, S. J.; Gallo, R. C.; Gallagher, R. E. Continuous growth and differentiation of human myeloid leukaemic cells in suspension culture. Nature. 270: 347–349; 1977. doi:10.1038/270347a0.

    Article  PubMed  CAS  Google Scholar 

  • Deshaies, R. J. SCF and Cullin/Ring H2-based ubiquitin ligases. Annu. Rev. Cell Dev. Biol. 15: 435–467; 1999. doi:10.1146/annurev.cellbio.15.1.435.

    Article  PubMed  CAS  Google Scholar 

  • Dias, D. C.; Dolios, G.; Wang, R.; Pan, Z. Q. CUL7: A DOC domain-containing cullin selectively binds Skp1·Fbx29 to form an SCF-like complex. Proc. Natl. Acad. Sci. U.S.A. 99: 16601–16606; 2002. doi:10.1073/pnas.252646399.

    Article  PubMed  CAS  Google Scholar 

  • Driouch, K.; Briffod, M.; Bièche, I.; Champème, M.-H.; Lidereau, R. Location of several putative genes possibly involved in human breast cancer progression. Cancer Res. 58: 2081–2086; 1998.

    PubMed  CAS  Google Scholar 

  • Duan, H.; Wang, Y.; Aviram, M.; Swaroop, M.; Loo, J. A.; Bian, J.; Tian, Y.; Mueller, T.; Bisgaier, C. L.; Sun, Y. SAG, a novel zinc RING finger protein that protects cells from apoptosis induced by redox agents. Mol. Cell Biol. 19: 3145–3155; 1999.

    PubMed  CAS  Google Scholar 

  • Fay, M. J.; Longo, K. A.; Karathanasis, G. A.; Shope, D. M.; Mandernach, C. J.; Leong, J. R.; Hicks, A.; Pherson, K.; Husain, A. Analysis of CUL-5 expression in breast epithelial cells, breast cancer cell lines, normal tissues and tumor tissues. Mol. Cancer 2: 40; 2003. doi:10.1186/1476-4598-2-40.

    Article  PubMed  Google Scholar 

  • Gallagher, R.; Collins, S.; Trujillo, J.; McCredie, K.; Ahearn, M.; Tsai, S.; Metzgar, R.; Aulakh, R.; Ting, F.; Ruscetti, F.; Gallo, R. Characterization of the continuous, differentiating myeloid cell line (HL-60) from a patient with acute promyelocytic leukemia. Blood. 54: 713–733; 1979.

    PubMed  CAS  Google Scholar 

  • Giguere, V. Retinoic acid receptors and cellular retinoid binding proteins: Complex interplay in retinoid signaling. Endocr. Rev. 15: 61–79; 1994. doi:10.1210/er.15.1.61.

    PubMed  CAS  Google Scholar 

  • Givan, A. L. The basics of staining for cell surface proteins. In: Diamond R.; DeMaggio S. (eds) In living color: protocols in flow cytometry and cell sorting. Springer, Berlin, pp 142–164; 2000.

    Google Scholar 

  • Gu, Q.; Tan, M.; Sun, Y. SAG/ROC2/Rbx2 is a novel activator protein-1 target that promotes c-Jun degradation and inhibits 12-O-tetradecanoylphorbol-13-acetate-induced neoplastic transformation. Cancer Res. 67: 3616–3625; 2007. doi:10.1158/0008-5472.CAN-06-4020.

    Article  PubMed  CAS  Google Scholar 

  • Gudmundsson, J.; Barkardottir, R. B.; Eiriksdottir, G.; Baldursson, T.; Arason, A.; Eglisson, V.; Ingvarsson, S. Loss of heterozygosity at chromosome 11 in breast cancer: Association of prognostic factors with genetic alterations. Br. J. Cancer 72: 696–701; 1995.

    PubMed  CAS  Google Scholar 

  • Guibal, F. C.; Moog-Lutz, C.; Smolewski, P.; Di Gioia, Y.; Darzynkiewicz, Z.; Lutz, P. G.; Cayre, Y. E. ASB-2 inhibits growth and promotes commitment in myeloid leukemia cells. J. Biol. Chem. 277: 218–224; 2002. doi:10.1074/jbc.M108476200.

    Article  PubMed  CAS  Google Scholar 

  • Hampton, G. M.; Mannermaa, A.; Winquist, R.; Alavaikko, M.; Blanco, G.; Taskinen, P. J.; Kiviniemi, H.; Newsham, I.; Cavanee, W. K.; Evans, G. A. Loss of heterozygosity in sporadic human breast carcinoma: A common region between 11q22 and 11q23.3. Cancer Res. 54: 4586–4589; 1994.

    PubMed  CAS  Google Scholar 

  • Harris, R.; Ralph, P. Human leukemic models of myelomonocytic development: A review of the HL-60 and U937 cell lines. J. Leukoc. Biol. 37: 407–422; 1985.

    PubMed  CAS  Google Scholar 

  • Hershko, A.; Ciechanover, A. The Ubiquitin System. Annu. Rev. Biochem. 67: 425–479; 1998. doi:10.1146/annurev.biochem.67.1.425.

    Article  PubMed  CAS  Google Scholar 

  • Heuze, M. L.; Guibal, F. C.; Banks, C. A.; Conaway, J. W.; Conaway, R. C.; Cayre, Y. E.; Benecke, A.; Lutz, P. G. ASB-2 is an Elongin BC-interacting protein that can assemble with Cullin 5 and Rbx1 to reconstitute an E3 ubiquitin ligase complex. J. Biol. Chem. 280: 5468–5474; 2005. doi:10.1074/jbc.M413040200.

    Article  PubMed  CAS  Google Scholar 

  • Heuze, M. L.; Lamsoul, I.; Baldassarre, M.; Lad, Y.; Leveque, S.; Razinia, Z.; Moog-Lutz, C.; Calderwood, D. A.; Lutz, P. G. ASB2 targets filamins A and B to proteasomal degradation. Blood. 2008, (in press). doi:10.1182/blood-2007-12-128744

  • Hilton, D. J.; Richardson, R. T.; Alexander, W. S.; Viney, E. M.; Wilson, T. A.; Sprigg, N. S.; Starr, R.; Nicholson, S. E.; Metcalf, D.; Nicola, N. A. Twenty proteins containing a C-terminal SOCS box form five structural classes. Proc. Natl. Acad. Sci. U.S.A. 95: 114–119; 1998. doi:10.1073/pnas.95.1.114.

    Article  PubMed  CAS  Google Scholar 

  • Huang, M. E.; Ye, Y. C.; Chen, S. R.; Chai, J. R.; Lu, J. X.; Zhoa, L.; Gu, L. J.; Wang, Z. Y. Use of all-trans retinoic acid in the treatment of acute promyelocytic leukemia. Blood. 72: 567–572; 1988.

    PubMed  CAS  Google Scholar 

  • Iwai, K.; Yamanaka, K.; Kamura, T.; Minato, N.; Conaway, R. C.; Conaway, J. W.; Klausner, R. D.; Pause A. Identification of the von Hippel-Lindau tumor-suppressor protein as part of an active E3 ubiquitin ligase complex. Proc. Natl. Acad. Sci. U.S.A. 96: 12436–12441; 1999. doi:10.1073/pnas.96.22.12436.

    Article  PubMed  CAS  Google Scholar 

  • Kalla, C.; Scheuermann, M. O.; Kube, I.; Schlotter, M.; Mertens, D.; Döhner, H.; Stilgenbauer, S.; Lichter, P. Analysis of 11q22-q23 deletion target genes in B-cell chronic lymphocytic leukaemia: Evidence for a pathogenic role of NPAT, CUL5, and PPP2R1B. Eur. J. Cancer 43: 1328–1335; 2007. doi:10.1016/j.ejca.2007.02.005.

    Article  PubMed  CAS  Google Scholar 

  • Kamura, T.; Burian, D.; Yan, Q.; Schmidt, S. L.; Lane, W. S.; Querido, E.; Branton, P. E.; Shilatifard, A.; Conaway, R. C.; Conaway, J. W. MUF1, a novel Elongin BC-interacting leucine-rich repeat protein that can assemble with Cul5 and Rbx1 to reconstitute a ubiquitin ligase. J. Biol. Chem. 276: 29748–2953; 2001. doi:10.1074/jbc.M103093200.

    Article  PubMed  CAS  Google Scholar 

  • Kamura, T.; Koepp, D. M.; Conrad, M. N.; Skowyra, D.; Moreland, R. J.; Iliopoulos, O.; Lane, W. S.; Kaelin, W. G. Jr.; Elledge, S. J.; Conaway, R. C.; Harper, J. W.; Conaway, J. W. Rbx1, a component of the VHL tumor suppressor complex and SCF ubiquitin ligase. Science. 284: 657–661; 1999. doi:10.1126/science.284.5414.657.

    Article  PubMed  CAS  Google Scholar 

  • Kamura, T.; Sato, S.; Haque, D.; Liu, L.; Kaelin, W. G. Jr; Conaway, R. C.; Conaway, J. W. The Elongin BC complex interacts with the conserved SOCS-box motif present in members of the SOCS, ras, WD-40 repeat, and ankyrin repeat families. Genes Dev. 12: 3872–3881; 1998. doi:10.1101/gad.12.24.3872.

    Article  PubMed  CAS  Google Scholar 

  • Kibel, A.; Iliopoulos, O.; DeCaprio, J. A.; Kaelin, W. G. Jr. Binding of the von Hippel-Lindau tumor suppressor protein to Elongin B and C. Science. 269: 1444–1446; 1995. doi:10.1126/science.7660130.

    Article  PubMed  CAS  Google Scholar 

  • Kile, B. T.; Schulman, B. A.; Alexander, W. S.; Nicola, N. A.; Martin, H. M. E.; Hilton, D. J. The SOCS box: a tale of destruction and degradation. Trends Biochem. Sci. 27: 235–241; 2002. doi:10.1016/S0968-0004(02)02085-6.

    Article  PubMed  CAS  Google Scholar 

  • Kile, B. T.; Viney, E. M.; Wilson, T. A.; Brodnicki, T. C.; Cancilla, M. R.; Herlihy, A. S.; Croker, B. A.; Baca, M.; Nicola, N. A.; Hilton, D. J.; Alexander, W. S. Cloning and characterization of the genes encoding the ankyrin repeat and SOCS box-containing proteins Asb-1, Asb-2, Asb-3 and Asb-4. Gene. 258: 31–41; 2000. doi:10.1016/S0378-1119(00)00402-9.

    Article  PubMed  CAS  Google Scholar 

  • Kipreos, E. T.; Lander, L. E.; Wing, J. P.; He, W. W.; Hedgecock, E. M. cul-1 is required for cell cycle exit in C. elegans and identifies a novel gene family. Cell. 85: 829–839; 1996. doi:10.1016/S0092-8674(00)81267-2.

    Article  PubMed  CAS  Google Scholar 

  • Kitareewan, S.; Pitha-Rowe, I.; Sekula, D.; Lowrey, C. H.; Nemeth, M. J.; Golub, T. R.; Freemantle, S. J.; Dimitrovsky, E. UBE1L is a retinoid target that triggers PML/RARα degradation and apoptosis in acute promyelocytic leukemia. Proc. Natl. Acad. Sci. U.S.A. 99: 3806–3811; 2002. doi:10.1073/pnas.052011299.

    Article  PubMed  CAS  Google Scholar 

  • Kohroki, J.; Fujita, S.; Itoh, N.; Yamada, Y.; Imai, H.; Yumoto, N.; Nakanishi, T.; Tanaka, K. ATRA-regulated ASB-2 gene induced in differentiation of HL-60 leukemia cells. FEBS Lett. 505: 223–228; 2001. doi:10.1016/S0014-5793(01)02829-0.

    Article  PubMed  CAS  Google Scholar 

  • Kohroki, J.; Nishiyama, T.; Nakamura, T.; Masuho, Y. ASB proteins interact with Cullin5 and Rbx2 to form E3 ubiquitin ligase complexes. FEBS Lett. 579: 6796–6802; 2005. doi:10.1016/j.febslet.2005.11.016.

    Article  PubMed  CAS  Google Scholar 

  • Krebs, D. L.; Hilton, D. J. SOCS: physiological suppressors of cytokine signaling. J. Cell Sci. 113: 2813–2819; 2000.

    PubMed  CAS  Google Scholar 

  • Laemmli, U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227: 680–685; 1970. doi:10.1038/227680a0.

    Article  PubMed  CAS  Google Scholar 

  • Li, B.; Yang, F. C.; Clapp, D. W.; Chun, K. T. Enforced expression of CUL-4A interferes with granulocytic differentiation and exit from the cell cycle. Blood. 101: 1769–1776; 2003. doi:10.1182/blood-2002-05-1517.

    Article  PubMed  CAS  Google Scholar 

  • Mathias, N.; Johnson, S. L.; Winey, M.; Adams, A. E. M.; Goetsch, L.; Pringle, J. R.; Byers, B.; Goebl, M. G. Cdc53p acts in concert with Cdc4p and Cdc34p to control the G1-to-S-phase transition and identifies a conserved family of proteins. Mol. Cell Biol. 16: 6634–6643; 1996.

    PubMed  CAS  Google Scholar 

  • Mayer, A. M. S.; Brenic, S.; Glaser, K. B. Pharmacological targeting of signaling pathways in protein kinase C-stimulated superoxide generation in neutrophil-like HL-60 cells: effect of phorbol ester, arachidonic acid and inhibitors of kinase(s), phosphatase(s) and phospholipase A2 1. J. Pharmacol. Exp. Ther. 279: 633–644; 1996.

    PubMed  CAS  Google Scholar 

  • Mayer, A. M. S.; Brenic, S.; Stocker, R.; Glaser, K. B. Modulation of superoxide generation in in vivo lipopolysaccharide-primed rat alveolar macrophages by arachidonic acid and inhibitors of protein kinase C, phospholipase A2, protein serine-threonine phosphatase(s), protein tyrosine kinases(s) and phosphatase(s). J. Pharmacol. Exp. Ther. 274: 427–436; 1995.

    PubMed  CAS  Google Scholar 

  • Negrini, M.; Rasio, D.; Hampton, G. M.; Sabbioni, S.; Rattan, S.; Carter, S. L.; Rosenberg, A. L.; Schwartz, G. F.; Shiloh, Y.; Cavenee, W. K.; Croce, C. M. Definition and refinement of chromosome 11 regions of loss of heterozygosity in breast cancer: Identification of a new region at 11q23.3. Cancer Res. 55: 3003–3007; 1995.

    PubMed  CAS  Google Scholar 

  • Nikolaev, A. Y.; Li, M.; Puskas, N.; Qin, J.; Gu, W. Parc: a cytoplasmic anchor for p53. Cell. 112: 29–40; 2003. doi:10.1016/S0092-8674(02)01255-2.

    Article  PubMed  CAS  Google Scholar 

  • Ohta, T.; Michel, J. J.; Schottelius, A. J.; Xiong, Y. ROC1, a homolog of APC11, represents a family of Cullin partners with an associated ubiquitin ligase activity. Mol. Cell. 3: 535–541; 1999a. doi:10.1016/S1097-2765(00)80482-7.

    Article  PubMed  CAS  Google Scholar 

  • Ohta, T.; Michel, J. J.; Xiong, Y. Association with cullin partners protects ROC proteins from proteasome-dependent degradation. Oncogene. 18: 6758–6766; 1999b. doi:10.1038/sj.onc.1203115.

    Article  PubMed  CAS  Google Scholar 

  • Ohta, T.; Xiong, Y. Phosphorylation- and SKP1-independent in vitro ubiquination of E2F1 by multiple ROC-Cullin ligases. Cancer Res. 61: 1347–1353; 2001.

    PubMed  CAS  Google Scholar 

  • Olins, A. L.; Olins, D. E. Cytoskeletal influences on nuclear shape in granulocytic HL-60 cells. BMC Cell Biol. 5: 30; 2004. doi:10.1186/1471-2121-5-30.

    Article  PubMed  CAS  Google Scholar 

  • Seol, J. H.; Feldman, R. M. R.; Zachariae, W.; Shevchenko, A.; Correll, C. C.; Lyapina, S.; Chi, Y.; Galova, M.; Claypool, J.; Sandmeyer, S.; Nasmyth, K.; Shevchenko, A.; Deshaies, R. J. Cdc53/cullin and the essential Hrt1 RING-H2 subunit of SCF define a ubiquitin ligase module that activates the E2 enzyme Cdc34. Genes Dev. 13: 1614–1626; 1999. doi:10.1101/gad.13.12.1614.

    Article  PubMed  CAS  Google Scholar 

  • Sun, Y.; Tan, M.; Duan, H.; Swaroop, M. SAG/ROC/Rbx/Hrt, a zinc RING finger gene family: Molecular cloning, biochemical properties, and biological functions. Antioxid. Redox. Signal 3: 635–650; 2001. doi:10.1089/15230860152542989.

    Article  PubMed  CAS  Google Scholar 

  • Tamayo, P.; Slonim, D.; Mesirov, J.; Zhu, Q.; Kitareewan, S.; Dmitrovsky, E.; Lander, E. S.; Golub, T. R. Interpreting patterns of gene expression with self-organizing maps: Methods and application to hematopoietic differentiation. Proc. Natl. Acad. Sci. U.S.A. 96: 2907–2912; 1999. doi:10.1073/pnas.96.6.2907.

    Article  PubMed  CAS  Google Scholar 

  • Tomlinson, I. P. M.; Strickland, J. E.; Lee, A. S. G.; Bromley, L.; Evans, M. F.; Morton, J.; McGee, J. O. D. Loss of hterozygosity on chromosome 11q in breast cancer. J. Clin. Pathol. 48: 424–428; 1995. doi:10.1136/jcp.48.5.424.

    Article  PubMed  CAS  Google Scholar 

  • Trayner, I. D.; Bustorff, T.; Etches, A. E.; Mufti, G. J.; Foss, Y.; Farzaneh, F. Changes in antigen expression on differentiating HL60 cells treated with dimetylsulphoxide, all-trans retinoic acid, α 1,25-dihydroxyvitamin D3 or 12-O-tetradecanoyl phorbol-13-acetate. Leuk. Res. 22: 537–547; 1998. doi:10.1016/S0145-2126(98)00041-1.

    Article  PubMed  CAS  Google Scholar 

  • Tsiftsoglou, A. S.; Robinson, S. H. Differentiation of Leukemic Cell Lines: A review focusing on Murine Erythroleukemia and Human HL-60 Cells. Int. J. Cell Cloning 3: 349–366; 1985.

    Article  PubMed  CAS  Google Scholar 

  • Van Dort, C.; Zhao, P.; Parmelee, K.; Capps, B.; Poel, A.; Listenberger, L.; Kossoris, J.; Wasilevich, B.; Murrey, D.; Clare, P.; Burnatowska-Hledin, M. VACM-1, a cul-5 gene, inhibits cellular growth by a mechanism that involves MAPK and p53 signaling pathways. Am. J. Physiol. Cell Physiol. 285: C1386–C1396; 2003.

    PubMed  Google Scholar 

  • Warrell, R. P. Jr; Frankel, S. R.; Miller, W. H.; Scheinberg, D. A.; Itri, L. M.; Hittelman, W. N.; Vyas, R.; Andreeff, M.; Tafuri, A.; Jakubowski, A.; Gabrilove, J.; Gordon, M. S.; Dmitrovsky, E. Differentiation therapy of acute promyelocytic leukemia with tretinoin (all-trans-retinoic acid). N. Engl. J. Med. 324: 1385–1393; 1991.

    PubMed  Google Scholar 

  • Willems, A. R.; Schwab, M.; Tyers, M. A hitchhiker’s guide to the cullin ubiquitin ligases: SCF and its kin. Biochim. Biophys. Acta 1695: 133–170; 2004. doi:10.1016/j.bbamcr.2004.09.027.

    Article  PubMed  CAS  Google Scholar 

  • Winqvist, R.; Hampton, G. M.; Mannermaa, A.; Blanco, G.; Alavaikko, M.; Kiviniemi, H.; Taskinen, P. J.; Evans, G. A.; Wright, F. A.; Newsham, I.; Cavenee, W. K. Loss of heterozygosity for chromosome 11 in primary human breast tumors is associated with poor survival after metastasis. Cancer Res. 55: 2660–2664; 1995.

    PubMed  CAS  Google Scholar 

  • Yang, G. Y.; Pang, L.; Ge, H. L.; Tan, M.; Ye, W.; Liu, X. H.; Huang, F. P.; Wu, D. C.; Che, X. M.; Song, Y.; Wen, R.; Sun, Y. Attenuation of ischemia-induced mouse brain injury by SAG, a redox-inducible antioxidant protein. J. Cereb. Blood Flow Metab. 21: 722–733; 2001. doi:10.1097/00004647-200106000-00010.

    Article  PubMed  CAS  Google Scholar 

  • Yao, X. L.; Liu, J.; Lee, E.; Ling, G. S. F.; McCabe, J. T. Cullin 5 gene expression in the rat cerebral cortex and hippocampus following traumatic brain injury (TBI). Neurosci. Lett. 409: 65–69; 2006. doi:10.1016/j.neulet.2006.09.015.

    Article  PubMed  CAS  Google Scholar 

  • Yu, H.; Peters, J. M.; King, R. W.; Page, A. M.; Hieter, P.; Kirschner, M. W. Identification of a cullin homology region in a subunit of the anaphase-promoting complex. Science. 279: 1219–22; 1998. doi:10.1126/science.279.5354.1219.

    Article  PubMed  CAS  Google Scholar 

  • Yuan, J. S.; Reed, A.; Chen, F.; Stewart, N. C. Jr. Statistical analysis of real-time PCR data. BMC Bioinformatics. 7: 85; 2006. doi:10.1186/1471-2105-7-85.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank the Robert H. Lurie Comprehensive Cancer Center Flow Cytometry Core Facility at Northwestern University and Dr. Alice Givan of the Englert Cell Analysis Laboratory at Dartmouth Medical School for assistance with the collection and analysis of the flow cytometry data. We also thank Dr. Nalini Chandar of the Biochemistry Department at Midwestern University for reviewing this manuscript prior to submission. This research was supported in part by the Biomedical Sciences Department and the Office of Research and Sponsored Programs at Midwestern University and by grant number R15 CA 122003-01 from the National Cancer Institute of the NIH.

Author information

Authors and Affiliations

  1. Department of Pharmacology, Chicago College of Osteopathic Medicine, Midwestern University, 555 31st Street, Downers Grove, IL, 60515, USA

    Shaneen S. Baxter, Lauren A. Carlson, Alejandro M. S. Mayer, Mary L. Hall & Michael J. Fay

  2. Department of Biomedical Sciences, College of Health Sciences, Midwestern University, 555 31st Street, Downers Grove, IL, 60515, USA

    Shaneen S. Baxter & Michael J. Fay

Authors
  1. Shaneen S. Baxter
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lauren A. Carlson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alejandro M. S. Mayer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mary L. Hall
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Michael J. Fay
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael J. Fay.

Additional information

Editor: J. Denry Sato

Rights and permissions

Reprints and permissions

About this article

Cite this article

Baxter, S.S., Carlson, L.A., Mayer, A.M.S. et al. Granulocytic differentiation of HL-60 promyelocytic leukemia cells is associated with increased expression of Cul5. In Vitro Cell.Dev.Biol.-Animal 45, 264–274 (2009). https://doi.org/10.1007/s11626-008-9163-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11626-008-9163-4

Keywords

Search

Navigation