Contribution of functional voltage‐gated Na+ channel expression to cell behaviors involved in the metastatic cascade in rat prostate cancer: II. Secretory membrane activity

Journal of Cellular Physiology - Tập 195 Số 3 - Trang 461-469 - 2003
Maria E. Mycielska1, Scott P. Fraser1, Marek Szatkowski2, Mustafa B.A. Djamgoz1
1Department of Biological Sciences, Sir Alexander Fleming Building, Imperial College of Science, Technology and Medicine, London, United Kingdom
2Division of Biomedical Sciences, Sir Alexander Fleming Building, Imperial College of Science, Technology and Medicine, London, United Kingdom

Tóm tắt

AbstractThe secretory membrane activities of two rat prostate cancer cell lines of markedly different metastatic potential, and corresponding electrophysiological characteristics, were studied in a comparative approach. In particular, voltage‐gated Na+ channels (VGSCs) were expressed in the strongly metastatic MAT‐LyLu but not in the closely related, but weakly metastatic, AT‐2 cells. Uptake and release of the non‐cytotoxic marker horseradish peroxidase (HRP) were used as indices of general endocytotic and exocytotic membrane activity, respectively. The amount of tracer present in a given experimental condition was quantified by light microscopic digital imaging. The uptake of HRP was an active process, abolished completely by incubating the cells at low temperature (5°C) and suppressed by disrupting the cytoskeleton. Interestingly, the extent of HRP uptake into the strongly metastatic MAT‐LyLu cells was almost twice that into the weakly metastatic AT‐2 cells. Vesicular uptake of HRP occurred in a fast followed by a slow phase; these appeared to correspond to cytoplasmic and perinuclear pools, respectively. Importantly, the overall quantitative difference in the uptake disappeared in the presence of 1 μM tetrodotoxin which significantly reduced the uptake of HRP into the MAT‐LyLu cells. There was no effect on the AT‐2 cells, consistent with functional VGSC expression occurring selectively in the former. A similar effect was observed in Na+‐free medium. The uptake was partially dependent upon extracellular Ca2+ but was not affected by raising the extracellular K+ concentration. We suggest that functional VGSC expression could potentiate prostate cancer cells' metastatic ability by enhancing their secretory membrane activity. © 2003 Wiley‐Liss, Inc.

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Tài liệu tham khảo

Abdul M, 2001, Inhibition by anticonvulsants of prostate‐specific antigen and interleukin‐6 secretion by human prostate cancer cells, Anticancer Res, 21, 2045

10.1111/j.1469-7793.1999.00033.x

Barbero MC, 1991, Correlation between secretion pattern and metastatic potential from drug‐treated 3ll tumor‐cell line, Cell Mol Biol, 37, 501

10.1113/jphysiol.1993.sp019472

10.1152/physrev.1999.79.3.763

10.1152/ajprenal.2000.278.2.F192

10.1111/j.1469-7793.2000.t01-2-00579.x

10.1016/S0959-8049(00)00094-0

10.1016/S0092-8674(01)00428-7

DingY.2001.PhD Thesis University of London.

Djamgoz MBA, 2001, Directional movement of rat prostate cancer cells in direct‐current electric field: Involvement of voltage‐gated Na+ channel activity, J Cell Sci, 114, 2697, 10.1242/jcs.114.14.2697

10.1523/JNEUROSCI.18-11-04029.1998

10.1111/j.1469-7793.1998.591bv.x

Farquhar MG, 1983, Multiple pathways of exocytosis, endocytosis, and membrane recycling—validation of a Golgi route, Fed Proc, 42, 2407

10.1016/S0962-8924(98)01316-6

Fraser SP, 1998, Voltage‐gated Na+ channel activity contributes to rodent prostate cancer migration in vitro, J Physiol, 513, 131P

10.1007/s004410051256

Freedman SD, 1999, Endocytosis at the apical plasma membrane of pancreatic acinar cells is regulated by tyrosine kinases, Am J Physiol, 276, C306, 10.1152/ajpcell.1999.276.2.C306

10.1007/s004180050287

10.1083/jcb.120.3.695

10.1002/(SICI)1097-4652(199804)175:1<50::AID-JCP6>3.0.CO;2-B

10.1016/0014-5793(95)00772-2

10.1111/j.1469-7793.1999.0745p.x

10.1038/35096054

10.1016/S0014-5793(99)00561-X

10.1016/0014-4835(91)90130-7

10.1111/j.1469-7793.2001.0141j.x

10.1111/j.1469-7793.1999.00023.x

10.1002/pros.2990090306

10.1073/pnas.96.17.9949

10.1113/jphysiol.1996.sp021475

Katz B, 1969, The release of neurotransmitter substances

10.1113/jphysiol.1967.sp008183

10.1111/j.1469-7793.2001.0771e.x

10.1006/bbrc.2001.4371

10.1054/mehy.1997.0637

10.1016/S0896-6273(00)80226-3

10.1074/jbc.272.33.20332

Laniado ME, 1997, Expression and functional analysis of voltage‐activated Na+ channels in human prostate cancer cell lines and their contribution to invasiveness in vitro, Am J Pathol, 150, 1213

10.1016/S0006-3495(99)77385-6

10.1111/j.1469-7793.1997.367be.x

10.1111/j.1469-7793.2001.0389a.x

10.1046/j.1471-4159.2000.0740367.x

10.1002/jlb.57.5.747

10.1242/jcs.113.7.1213

10.1523/JNEUROSCI.18-01-00081.1998

10.1016/S1357-4310(00)01686-5

10.1111/j.1469-7793.1998.219bf.x

Morgan A, 1995, Exocytosis, Essays Biochem, 30, 77

10.1016/S0167-0115(97)01075-6

10.1023/A:1005531100458

Mycielska M, 2001, Endocytic membrane activity in rat prostate cancer cell lines: Potentiation by functional voltage‐gated sodium channels, J Physiol, 531, 81P

10.1016/S0014-5793(00)02151-7

10.1016/S0955-0674(97)80025-7

10.1074/jbc.M104927200

10.1083/jcb.150.5.F111

10.1113/jphysiol.1996.sp021474

10.1111/j.1469-7793.1997.105bl.x

10.1016/S0896-6273(00)00065-9

10.1126/science.278.5344.1728

10.1038/297079a0

Rothman JE, 1995, Molecular mechanisms of intracellular protein‐transport, FASEB J, 9, A1458

10.1083/jcb.70.1.178

10.1016/S0014-5793(98)00050-7

10.1083/jcb.148.4.755

10.1152/ajpcell.1999.277.6.C1239

10.1006/scbi.1996.0020

10.1159/000016372

10.1083/jcb.70.2.294

10.1002/j.1460-2075.1993.tb05657.x

10.1113/jphysiol.1991.sp018418

10.1016/S0300-9084(00)00193-0

Verheugen JA, 1994, Veratridine blocks voltage‐gated potassium current in human T lymphocytes and in mouse neuroblastoma cells, J Membr Biol, 137, 205

Walsh JH, 1991, Autocrine growth factors and solid tumor malignancy, West J Med, 155, 152

10.1111/j.1469-7793.2001.0405k.x

10.1016/S0896-6273(00)80208-1

10.2307/3580324

10.1172/JCI9258

10.1111/j.1469-7793.1999.0461v.x

10.1128/MCB.20.21.8069-8083.2000