Skip to main content
Log in

An intermediate-conductance Ca2+-activated K+ channel mediates B lymphoma cell cycle progression induced by serum

  • Cell and Molecular Physiology
  • Published:
Pflügers Archiv - European Journal of Physiology Aims and scope Submit manuscript

Abstract

We have previously reported that Kv1.3 channel is expressed in Daudi cells. However, the present study demonstrates that Daudi cell cycle progression is not affected by margatoxin, a Kv1.3 channel blocker, but can be suppressed by tetraethylammonium (TEA) and 1-[(2-chlorophenyl) diphenylmethyl]-1H-pyrazole (TRAM-34), a selective blocker of intermediate-conductance Ca2+-activated K+ (IK) channels. Our patch-clamp data indicate that Daudi cells express an IK channel because it has a unit conductance of about 30 pS, is voltage-independent, and can be activated by submicromolar Ca2+ and blocked by TRAM-34. Fetal bovine serum (FBS) elevated intracellular Ca2+ concentration ([Ca2+]i) and activated this IK channel. Conversely, Rituximab, a human–mouse chimeric monoclonal antibody of CD20, significantly decreased [Ca2+]i and inhibited the channel. Furthermore, both FBS-induced IK channel expression and cell cycle progression were attenuated by the treatment with LY-294002, a phosphatidylinositol 3-kinase (PI3K) inhibitor. These data together suggest that a growth factor(s) in FBS triggers cell cycle progression by elevating both IK channel activity via CD20 and IK channel expression on the cell surface via PI3K. Thus, elevated IK channel activity and expression may account, in part, for Daudi cell malignant growth and proliferation.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Avivi I, Robinson S, Goldstone A (2003) Clinical use of rituximab in haematological malignancies. Br J Cancer 89:1389–1394

    Article  PubMed  CAS  Google Scholar 

  2. Beck TW, Magnuson NS, Rapp UR (1995) Growth factor regulation of cell cycle progression and cell fate determination. Curr Top Microbiol Immunol 194:291–303

    PubMed  CAS  Google Scholar 

  3. Berridge MJ (1995) Calcium signalling and cell proliferation. BioEssays 17:491–500

    Article  PubMed  CAS  Google Scholar 

  4. Bloch M, Ousingsawat J, Simon R, Schraml P, Gasser TC, Mihatsch MJ, Kunzelmann K, Bubendorf L (2006) KCNMA1 gene amplification promotes tumor cell proliferation in human prostate cancer. Oncogene DOI 10.1038/sj.onc.1210036 (in press)

  5. Bubien JK, Zhou LJ, Bell PD, Frizzell RA, Tedder TF (1993) Transfection of the CD20 cell surface molecule into ectopic cell types generates a Ca2+ conductance found constitutively in B lymphocytes. J Cell Biol 121:1121–1132

    Article  PubMed  CAS  Google Scholar 

  6. Chang KL, Kamel OW, Arber DA, Horyd ID, Weiss LM (1995) Pathologic features of nodular lymphocyte predominance Hodgkin’s disease in extranodal sites. Am J Surg Pathol 19:1313–1324

    Article  PubMed  CAS  Google Scholar 

  7. Coiret G, Borowiec AS, Mariot P, Ouadid-Ahidouch H, Matifat F (2006) The antiestrogen tamoxifen activates BK channels and stimulates proliferation of MCF-7 breast cancer cells. Mol Pharmacol 71:843–851

    Article  PubMed  CAS  Google Scholar 

  8. Conforti L, Petrovic M, Mohammad D, Lee S, Ma Q, Barone S, Filipovich AH (2003) Hypoxia regulates expression and activity of Kv1.3 channels in T lymphocytes: a possible role in T cell proliferation. J Immunol 170:695–702

    PubMed  CAS  Google Scholar 

  9. DeCoursey TE, Chandy KG, Gupta S, Cahalan MD (1984) Voltage-gated K+ channels in human T lymphocytes: a role in mitogenesis?. Nature 307:465–468

    Article  PubMed  CAS  Google Scholar 

  10. Fanger CM, Rauer H, Neben AL, Miller MJ, Rauer H, Wulff H, Rosa JC, Ganellin CR, Chandy KG, Cahalan MD (2001) Calcium-activated potassium channels sustain calcium signaling in T lymphocytes. Selective blockers and manipulated channel expression levels. J Biol Chem 276:12249–12256

    Article  PubMed  CAS  Google Scholar 

  11. Gallagher JD, Noelle RJ, McCann FV (1995) Mercury suppression of a potassium current in human B lymphocytes. Cell Signal 7:31–38

    Article  PubMed  CAS  Google Scholar 

  12. Gamper N, Fillon S, Huber SM, Feng Y, Kobayashi T, Cohen P, Lang F (2002) IGF-1 up-regulates K+ channels via PI3-kinase, PDK1 and SGK1. Pflugers Arch 443:625–634

    Article  PubMed  CAS  Google Scholar 

  13. Gongora R, Stephan RP, Zhang Z, Cooper MD (2001) An essential role for Daxx in the inhibition of B lymphopoiesis by type I interferons. Immunity 14:727–737

    Article  PubMed  CAS  Google Scholar 

  14. Grgic I, Eichler I, Heinau P, Si H, Brakemeier S, Hoyer J, Kohler R (2005) Selective blockade of the intermediate-conductance Ca2+-activated K+ channel suppresses proliferation of microvascular and macrovascular endothelial cells and angiogenesis in vivo. Arterioscler Thromb Vasc Biol 25:704–709

    Article  PubMed  CAS  Google Scholar 

  15. Grimberg A (2003) Mechanisms by which IGF-I may promote cancer. Cancer Biol Ther 2:630–635

    PubMed  CAS  Google Scholar 

  16. Helms MN, Liu L, Liang YY, Al-Khalili O, Vandewalle A, Saxena S, Eaton DC, Ma HP (2005) Phosphatidylinositol 3,4,5-trisphosphate mediates aldosterone stimulation of epithelial sodium channel (ENaC) and interacts with γ-ENaC. J Biol Chem 280:40885–40891

    Article  PubMed  CAS  Google Scholar 

  17. Jager H, Dreker T, Buck A, Giehl K, Gress T, Grissmer S (2004) Blockage of intermediate-conductance Ca2+-activated K+ channels inhibit human pancreatic cancer cell growth in vitro. Mol Pharmacol 65:630–638

    Article  PubMed  Google Scholar 

  18. Jensen BS, Odum N, Jorgensen NK, Christophersen P, Olesen SP (1999) Inhibition of T cell proliferation by selective block of Ca2+-activated K+ channels. Proc Natl Acad Sci USA 96:10917–10921

    Article  PubMed  CAS  Google Scholar 

  19. Ju YK, Wu MJ, Chaulet H, Marciniec T, Graham RM, Allen DG (2003) IGF-1 enhances a store-operated Ca2+ channel in skeletal muscle myoblasts: involvement of a CD20-like protein. J Cell Physiol 197:53–60

    Article  PubMed  CAS  Google Scholar 

  20. Kanzaki M, Nie L, Shibata H, Kojima I (1997) Activation of a calcium-permeable cation channel CD20 expressed in Balb/c 3T3 cells by insulin-like growth factor-I. J Biol Chem 272:4964–4969

    Article  PubMed  CAS  Google Scholar 

  21. Kanzaki M, Shibata H, Mogami H, Kojima I (1995) Expression of calcium-permeable cation channel CD20 accelerates progression through the G1 phase in Balb/c 3T3 cells. J Biol Chem 270:13099–13104

    PubMed  CAS  Google Scholar 

  22. Kojima I, Matsunaga H, Kurokawa K, Ogata E, Nishimoto I (1988) Calcium influx: an intracellular message of the mitogenic action of insulin-like growth factor-I. J Biol Chem 263:16561–16567

    PubMed  CAS  Google Scholar 

  23. Kwon G, Marshall CA, Liu H, Pappan KL, Remedi MS, McDaniel ML (2006) Glucose-stimulated DNA synthesis through mammalian target of rapamycin (mTOR) is regulated by KATP channels: effects on cell cycle progression in rodent islets. J Biol Chem 281:3261–3267

    Article  PubMed  CAS  Google Scholar 

  24. Liebau S, Propper C, Bockers T, Lehmann-Horn F, Storch A, Grissmer S, Wittekindt OH (2006) Selective blockage of Kv1.3 and Kv3.1 channels increases neural progenitor cell proliferation. J Neurochem 99:426–437

    Article  PubMed  CAS  Google Scholar 

  25. Lu X, Fein A, Feinstein MB, O’Rourke FA (1999) Antisense knock out of the inositol 1,3,4,5-tetrakisphosphate receptor GAP1(IP4BP) in the human erythroleukemia cell line leads to the appearance of intermediate conductance KCa channels that hyperpolarize the membrane and enhance calcium influx. J Gen Physiol 113:81–96

    Article  PubMed  CAS  Google Scholar 

  26. Ma H, Ling BN (1996) Luminal adenosine receptors regulate amiloride-sensitive Na channels in A6 distal nephron cells. Am J Physiol 270:F798–F805

    PubMed  CAS  Google Scholar 

  27. Malhi H, Irani AN, Rajvanshi P, Suadicani SO, Spray DC, McDonald TV, Gupta S (2000) KATP channels regulate mitogenically induced proliferation in primary rat hepatocytes and human liver cell lines. Implications for liver growth control and potential therapeutic targeting. J Biol Chem 275:26050–26057

    Article  PubMed  CAS  Google Scholar 

  28. McCann FV, McCarthy DC, Noelle RJ (1990) Patch-clamp profile of ion channels in resting murine B lymphocytes. J Membr Biol 114:175–188

    Article  PubMed  CAS  Google Scholar 

  29. Nolan MK, Jankowska L, Prisco M, Xu S, Guvakova MA, Surmacz E (1997) Differential roles of IRS-1 and SHC signaling pathways in breast cancer cells. Int J Cancer 72:828–834

    Article  PubMed  CAS  Google Scholar 

  30. Ouadid-Ahidouch H, Roudbaraki M, Delcourt P, Ahidouch A, Joury N, Prevarskaya N (2004) Functional and molecular identification of intermediate-conductance Ca2+-activated K+ channels in breast cancer cells: association with cell cycle progression. Am J Physiol 287:C125–C134

    Article  CAS  Google Scholar 

  31. Pardo LA (2004) Voltage-gated potassium channels in cell proliferation. Physiology 19:285–292

    Article  PubMed  CAS  Google Scholar 

  32. Partiseti M, Choquet D, Diu A, Korn H (1992) Differential regulation of voltage- and calcium-activated potassium channels in human B lymphocytes. J Immunol 148:3361–3368

    PubMed  CAS  Google Scholar 

  33. Press OW, Farr AG, Borroz KI, Anderson SK, Martin PJ (1989) Endocytosis and degradation of monoclonal antibodies targeting human B-cell malignancies. Cancer Res 49:4906–4912

    PubMed  CAS  Google Scholar 

  34. Stiles CD, Capone GT, Scher CD, Antoniades HN, Van Wyk JJ, Pledger WJ (1979) Dual control of cell growth by somatomedins and platelet-derived growth factor. Proc Natl Acad Sci USA 76:1279–1283

    Article  PubMed  CAS  Google Scholar 

  35. Sutro JB, Vayuvegula BS, Gupta S, Cahalan MD (1989) Voltage-sensitive ion channels in human B lymphocytes. Adv Exp Med Biol 254:113–122

    PubMed  CAS  Google Scholar 

  36. Tedder TF, Engel P (1994) CD20: a regulator of cell-cycle progression of B lymphocytes. Immunol Today 15:450–454

    Article  PubMed  CAS  Google Scholar 

  37. Wilker E, Lu J, Rho O, Carbajal S, Beltran L, DiGiovanni J (2005) Role of PI3K/Akt signaling in insulin-like growth factor-1 (IGF-1) skin tumor promotion. Mol Carcinog 44:137–145

    Article  PubMed  CAS  Google Scholar 

  38. Wonderlin WF, Strobl JS (1996) Potassium channels, proliferation and G1 progression. J Membr Biol 154:91–107

    Article  PubMed  CAS  Google Scholar 

  39. Wonderlin WF, Woodfork KA, Strobl JS (1995) Changes in membrane potential during the progression of MCF-7 human mammary tumor cells through the cell cycle. J Cell Physiol 165:177–185

    Article  PubMed  CAS  Google Scholar 

  40. Yamazaki D, Aoyama M, Ohya S, Muraki K, Asai K, Imaizumi Y (2006) Novel functions of small conductance Ca2+-activated K+ channel in enhanced cell proliferation by ATP in brain endothelial cells. J Biol Chem 281:38430–38439

    Article  PubMed  CAS  Google Scholar 

  41. Zhou ZH, Unlap MT, Li L, Ma H (2002) Incomplete inactivation of voltage-dependent potassium channels in human B lymphoma cells. J Membr Biol 188:97–105

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgement

This research was supported by DHHS, National Institutes of Health (NIH) Grant R01-DK067110 (to H.-P.M.)

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to He-Ping Ma.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, J., Xu, YQ., Liang, YY. et al. An intermediate-conductance Ca2+-activated K+ channel mediates B lymphoma cell cycle progression induced by serum. Pflugers Arch - Eur J Physiol 454, 945–956 (2007). https://doi.org/10.1007/s00424-007-0258-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00424-007-0258-7

Keywords

Navigation