Українська English

ISSN 2522-9028 (Print)
ISSN 2522-9036 (Online)
DOI: https://doi.org/10.15407/fz

Fiziologichnyi Zhurnal

is a scientific journal issued by the

Bogomoletz Institute of Physiology
National Academy of Sciences of Ukraine

Editor-in-chief: V.F. Sagach

The journal was founded in 1955 as
1955 – 1977 "Fiziolohichnyi zhurnal" (ISSN 0015 – 3311)
1978 – 1993 "Fiziologicheskii zhurnal" (ISSN 0201 – 8489)
1994 – 2016 "Fiziolohichnyi zhurnal" (ISSN 0201 – 8489)
2017 – "Fiziolohichnyi zhurnal" (ISSN 2522-9028)

Fiziol. Zh. 2007; 53(4): 110-128


Calcium signaling in carcinogenesis

Ia. M. Shuba.

    International Center of Molecular Physiology, NationalAcademy of Sciences of Ukraine



Abstract

Malignant transformation of the cells in cancer is caused by excessive proliferation accompanied by diminished ability for apoptosis due to the loss of normal control on these pro- cesses. Despite their ubiquity calcium ions are central to both processes, serving as major signalling agents. The present review examines what changes in calcium distribution among various compartments: extracellular space, cytoplasm, endoplasmic reticulum and mitochondria take place during transition from normal to pathological cell growth and death, what Ca2+-han- dling proteins are involved, and how this affects spatial and temporal characteristics of Ca2+ signals aimed at regulating specific cellular responses. Uncovering the underlying mo- lecular events may help elaborating new strategies for cancers treatment.

References

  1. Aaronson S. Growth factors and cancer // Science. – 1991. – 254. – Р.1146–1153.
  2. Allbritton N., Meyer T., Stryer L. Range of messenger action of calcium ion and inositol 1,4,5-trisphosphate // Ibid. – 1992. – 258. – P. 1812–1815.
  3. Altznauer F., Conus S., Cavalli A. et al. Calpain-1 regulates Bax and subsequent Smac-dependent caspase- 3 activation in neutrophil apoptosis // J. Biol. Chem. – 2004. – 279. – P. 5947–5957.
  4. Antonsson B., Martinou J. The Bcl-2 protein family / /Exp. Cell. Res. –2000. – 256. – P. 50–57.
  5. Benali-Furet N., Chami M., Houel L. et al. Hepatitis C virus core triggers apoptosis in liver cells by inducing ER stress and ER calcium depletion // Oncogene. – 2004. – 24. – P. 4921–4933.
  6. Benning C., Kyprianou N. Quinazoline-derived alpha1- adrenoceptor antagonists induce prostate cancer cell apoptosis via an alpha1-adrenoceptor-independent action // Cancer. Res. – 2002. – 62. – P. 597–602.
  7. Berridge M. Calcium signalling and cell proliferation / / Bioessays. – 1995. – 17. – P. 491–500.
  8. Berridge M., Bootman M., Lipp P. Calcium-a life and death signal //Nature. – 1998. – 395. – P. 645–648.
  9. 9. Berridge M., Bootman M., Roderick H. Calcium sig- nalling: dynamics, homeostasis and remodelling // Nat. Rev. Mol. Cell. Biol. – 2003. – 4. – P. 517–529.
  10. 10. Blaustein M.,Lederer W. Sodium/calcium exchange: its physiological implications // Physiol Rev. – 1999. – 79. – P. 763–854.
  11. Bobe R., Bredoux R., Corvazier E. et al. How many Ca(2)+ATPase isoforms are expressed in a cell type? A growing family of membrane proteins illustrated by studies in platelets // Platelets. – 2005. – 16. – P. 133–150.
  12. Bouillon R., Van Cromphaut S., Carmeliet G. Intesti- nal calcium absorption: Molecular vitamin D mediated mechanisms // J. Cell. Biochem. – 2003. – 88. – P. 332–339.
  13. Brechot C., Gozuacik D., Murakami Y., Paterlini- Brechot P. Molecular bases for the development of hepatitis B virus (HBV)-related hepatocellular carcinoma (HCC) // Semin. Cancer. Biol. – 2000. – 10. – P. 211–231.
  14. Brini M., Bano D., Manni S. et al. Effects of PMCA and SERCA pump overexpression on the kinetics of cell Ca(2+) signalling // Embo J. – 2000. – 19. – P. 4926–4935.
  15. Brouland J., Gelebart P., Kovacs T. et al. The loss of sarco/endoplasmic reticulum calcium transport ATPase 3 expression is an early event during the multistep process of colon carcinogenesis // Amer. J. Pathol. – 2005. – 167. – P. 233–242.
  16. Buchholz M., Schatz A., Wagner M.et al. Overexp- ression of c-myc in pancreatic cancer caused by ec- topic activation of NFATc1 and the Ca2+/calcineurin signaling pathway // Embo J. – 2005. – 25. – P. 3714–3724.
  17. Carafoli E. Biogenesis: plasma membrane calcium AT- Pase: 15 years of work on the purified enzyme // Faseb J. – 1994. – 8. – P. 993–1002.
  18. Chami M., Ferrari D., Nicotera P. et al. Caspase-de- pendent alterations of Ca2+ signaling in the induction of apoptosis by hepatitis B virus X protein // J. Biol. Chem. – 2003. – 278. – P. 31745–31755.
  19. 19. Chami M., Gozuacik D., Lagorce D. et al. SERCA1 trun- cated proteins unable to pump calcium reduce the endo- plasmic reticulum calcium concentration and induce apoptosis // J. Cell. Biol. – 2001. – 153. – P. 1301–1314.
  20. 20. Chami M., Gozuacik D., Saigo K. et al. Hepatitis B virus-related insertional mutagenesis implicates SERCA1 gene in the control of apoptosis // Oncogene. – 2000. – 19. – P. 2877–2886.
  21. Chen L., Fischle W., Verdin E., Greene W. Duration of nuclear NF-kappaB action regulated by reversible acety- lation // Science. – 2001. – 293. – P. 1653–1657.
  22. Chen L., Wang L., Zhu L. et al. Cell cycle-dependent expression of volume-activated chloride currents in nasopharyngeal carcinoma cells // Amer. J. Physiol. Cell. Physiol. – 2002. – 283. – P. C1313–1323.
  23. Chia V., Newcomb P. Calcium and colorectal cancer: some questions remain // Nutr Rev. – 2004. – 62. – P. 115–120.
  24. Clapham D. TRP channels as cellular sensors // Na- ture. – 2003. – 426. – P. 517–524.
  25. Colombo M., Sangiovanni A. Etiology, natural history and treatment of hepatocellular carcinoma // Antiviral Res. – 2003. – 60. – P. 145–150.
  26. Cooper G., Brostrom C., Brostrom M. Analysis of the endoplasmic reticular Ca2+ requirement for alpha1-an- titrypsin processing and transport competence // Biochem J. – 1997. – 325 ( Pt 3). – P. 601–608.
  27. Crabtree G. Calcium, calcineurin, and the control of tran- scription //J. Biol. Chem. – 2001. – 276. – P. 2313–2316.
  28. Dejmek J., Safholm A., Kamp Nielsen C. et. al. Wnt- 5a/Ca2+-induced NFAT activity is counteracted by Wnt- 5a/Yes-Cdc42–casein kinase 1alpha signaling in human mammary epithelial cells // Mol. Cell. Biol. – 2006. – 26. – P. 6024–6036.
  29. 29. Delgado-Coello B., Santiago–Garcia J., Zarain- Herzberg A., Mas-Oliva J. Plasma membrane Ca2+- ATPase mRNA expression in murine hepatocarcinoma and regenerating liver cells // Mol. Cell. Biochem. – 2003. – 247. – P. 177–184.
  30. 30. Denmeade S., Isaacs J. The SERCA pump as a thera- peutic target: making a «smart bomb» for prostate cancer // Cancer. Biol. Therap. – 2005. – 4. – P. 14–22.
  31. Denmeade S. , Jakobsen C., Janssen S. et. al. Prostate- specific antigen–activated thapsigargin prodrug as tar- geted therapy for prostate cancer // J. Natl. Cancer. Inst. – 2003. – 95. – P. 990–1000.
  32. Diaz–Horta O., Kamagate A., Herchuelz A., Van Eylen F. Na/Ca exchanger overexpression induces endoplas- mic reticulum-related apoptosis and caspase-12 acti- vation in insulin-releasing BRIN-BD11 cells // Diabe- tes. – 2002. – 51. – P. 1815–1824.
  33. Diaz–Horta O., Van Eylen F., Herchuelz A. Na/Ca ex- changer overexpression induces endoplasmic reticulum stress, caspase-12 release, and apoptosis // Ann N. Y. Acad Sciю. – 2003. – 1010. – P. 430–432.
  34. Dolmetsch R., Lewis R., Goodnow C., Healy J. Dif- ferential activation of transcription factors induced by Ca2+ response amplitude and duration // Nature. – 1997. – 386. – P. 855–858.
  35. Doroshenko P., Sabanov V., Doroshenko N. Cell cycle- related changes in regulatory volume decrease and vol- ume-sensitive chloride conductance in mouse fibro- blasts // J. Cell. Physiol. – 2001. – 187. – P. 65–72.
  36. Enfissi A., Prigent S., Colosetti P., Capiod T. The block- ing of capacitative calcium entry by 2-aminoethyl diphenylborate (2-APB) and carboxyamidotriazole (CAI) inhibits proliferation in Hep G2 and Huh-7 human hepatoma cells // Cell. Calcium. – 2004. – 36. – P. 459–467.
  37. Fixemer T., Wissenbach U., Flockerzi V., Bonkhoff H. Expression of the Ca2+-selective cation channel TRPV6 in human prostate cancer: a novel prognostic marker for tumor progression // Oncogene. – 2003. – 22. – P. 7858–7861.
  38. Gelebart P., Kovacs T., Brouland J. et.al. Expression of endomembrane calcium pumps in colon and gastric cancer cells. Induction of SERCA3 expression during differentiation // J. Biol. Chem. – 2002. – 277. – P. 26310–26320.
  39. 39. Giannini C., Brechot C. Hepatitis C virus biology //Cell. Death. Differ. – 2003. – 10 Suppl 1. – P. 527–538.
  40. 40. Gilabert J., Parekh A. Respiring mitochondria deter- mine the pattern of activation and inactivation of the store-operated Ca(2+) current I(CRAC) // Embo J. – 2002. – 19. – P. 6401–6407.
  41. Gill D., Waldron R., Rys-Sikora K. et al. Calcium pools, calcium entry, and cell growth // Biosci Rep. – 1996. – 16. – P. 139–157.
  42. Golovina V. Cell proliferation is associated with enhanced capacitative Ca(2+) entry in human arterial myocytes // Amer. J. Physiol. – 1999. – 277. – P. C343–349.
  43. Golovina V., Platoshyn O., Bailey C. et.al. Upregulated TRP and enhanced capacitative Ca(2+) entry in human pulmonary artery myocytes during proliferation // Amer. J. Physiol. Heart. Circulat. Physiol. – 2001. – 280. – P. 746–755.
  44. Gray L., Macdonald T. The pharmacology and regulation of T type calcium channels: new opportuni- ties for unique therapeutics for cancer // Cell. Calcium. – 2006. – 40. – P. 115–120.
  45. Guzey M., Kitada S., Reed J. Apoptosis induction by 1alpha,25-dihydroxyvitamin D3 in prostate cancer // Mol. Cancer. Therap. – 2002. – 1. – P. 667–677.
  46. Holmuhamedov E., Lewis L., Bienengraeber M. et.al. Suppression of human tumor cell proliferation through mitochondrial targeting // Faseb. J. – 2002. – 16. – P. 1010–1016.
  47. Hoth M., Button D., Lewis R. Mitochondrial control of calcium-channel gating: a mechanism for sustained signaling and transcriptional activation in T lympho- cytes // Proc. Natl. Acad. Sci. USA. – 2000. – 97. – P. 10607–10612.
  48. Hoth M., Fanger C., Lewis R. Mitochondrial regulation of store-operated calcium signaling in T lymphocytes // J. Cell. Biol. – 1997. – 137. – P. 633–648.
  49. 49. Huang Y., Chueh S., Teng C., Guh J. Investigation of ouabain-induced anticancer effect in human androgen- independent prostate cancer PC-3 cells //Biochem. Pharmacol. – 2004. – 67. – P. 727–733.
  50. 50. Humez S., Legrand G., Vanden-Abeele F. et.al. Role of endoplasmic reticulum calcium content in prostate cancer cell growth regulation by IGF and TNFalpha // J. Cell. Physiol. – 2004. – 201. – P. 201–213.
  51. Ihara E., Hirano K., Hirano M. et.al. Mechanism of down-regulation of L-type Ca(2+) channel in the pro- liferating smooth muscle cells of rat aorta // J. Cell. Biochem. – 2002. – 87. – P. 242–251.
  52. John L. , Lechleiter J., Camacho P. Differential modu- lation of SERCA2 isoforms by calreticulin // J. Cell. Biol. – 1998. – 142. – P. 963–973.
  53. Kahl C., Means A. Regulation of cell cycle progression by calcium/calmodulin-dependent pathways // Endocr. Rev. – 2003. – 24. – P. 719–736.
  54. Kallay E., Bajna E., Wrba F. et al. Dietary calcium and growth modulation of human colon cancer cells: role of the extracellular calcium–sensing receptor // Cancer. Detect. Prev. – 2000. – 24. – P. 127–136.
  55. Kirichok Y., Krapivinsky G., Clapham D. The mito- chondrial calcium uniporter is a highly selective ion channel // Nature. – 2004. – 427. – P. 360–364.
  56. Kushmerick C., Romano-Silva M., Gomez M., Prado M. Changes in Ca(2+) channel expression upon dif- ferentiation of SN56 cholinergic cells // Brain. Res. – 2001. – 916. – P. 199–210.
  57. Kyprianou N., Benning C. Suppression of human pros- tate cancer cell growth by alpha1-adrenoceptor antago- nists doxazosin and terazosin via induction of apop- tosis // Cancer. Res. – 2000a. – 60. – P. 4550–4555.
  58. Kyprianou N., Chon J., Benning C. Effects of Alpha(1)- adrenoceptor (alpha(1)-AR) antagonists on cell pro- liferation and apoptosis in the prostate: therapeutic implications in prostatic disease [In Process Citation] // Prostate Suppl. – 2000b. – 9. – P. 42–46.
  59. 59. Lamprecht S., Lipkin M. Chemoprevention of colon cancer by calcium, vitamin D and folate: molecular mechanisms // Nat. Rev. Cancer. – 2003. – 3. – P. 601–614.
  60. 60. Lang F., Ritter M., Gamper N. et. al. Cell volume in the regulation of cell proliferation and apoptotic cell death // Cell. Physiol. Biochem. – 2000. – 10. – P. 417–428.
  61. Laplante J., O’Rourke F., Lu X. et. al. Cloning of human Ca2+ homoeostasis endoplasmic reticulum protein (CHERP): regulated expression of antisense cDNA depletes CHERP, inhibits intracellular Ca2+ mobili- zation and decreases cell proliferation // Biochem J. – 2000. – 348 Pt 1. – P. 189–199.
  62. Lee J. , Park S., Lee M. et. al. Growth inhibition of human cancer cells in vitro by T-type calcium channel blockers // Bioorg. Med. Chem. Lett. – 2006. – 16. – P. 5014–5017.
  63. Lee W., Roberts-Thomson S. , Holman N. et. al. Ex- pression of plasma membrane calcium pump isoform mRNAs in breast cancer cell lines // Cell. Signal. – 2002. – 14. – P. 1015–1022.
  64. Lee W., Roberts-Thomson S., Monteith G. Plasma membrane calcium-ATPase 2 and 4 in human breast cancer cell lines // Biochem. and Biophys. Res. Commun. – 2005a. – 337. – P. 779–783.
  65. Lee W., Robinson J., Holman N. et. al. Antisense-me- diated Inhibition of the plasma membrane calcium- ATPase suppresses proliferation of MCF-7 cells // J. Biol. Chem. – 2005b. – 280. – P. 27076–27084.
  66. Lee Y., Kang-Park S., Do S. The hepatitis B virus-X protein activates a phosphatidylinositol 3-kinase-de- pendent survival signaling cascade // J. Biol. Chem. – 2001. – 276. – P. 16969–16977.
  67. Legrand G., Humez S., Slomianny C. et. al. Ca2+ pools and cell growth. Evidence for sarcoendoplasmic Ca2+- ATPases 2B involvement in human prostate cancer cell growth control // J. Biol. Chem. – 2001. – 276. – P. 47608–47614.
  68. Lemonnier L., Prevarskaya N., Shuba Y. et. al. Ca2+ modulation of volume-regulated anion channels: evi- dence for colocalization with store-operated channels // Faseb J. –2 002. – 16. – P. 222–224.
  69. 69. Lemonnier L., Shuba Y., Crepin A. et. al. Bcl-2-depen- dent modulation of swelling-activated Cl- current and ClC-3 expression in human prostate cancer epithelial cells // Cancer. Res. – 2004. – 64. – P. 4841–4848.
  70. 70. Li X., Stark G. R. NFkappaB-dependent signaling path- ways // Exp. Hematol. – 2002. – 30. – P. 285–296.
  71. Lipkin M., Newmark H. Vitamin D, calcium and pre- vention of breast cancer: a review // J. Amer. Coll. Nutr.– 1999.– 18. – P. 392S–397S.
  72. Lipskaia L., del Monte F., Capiod T. et. al. Sarco/en- doplasmic reticulum Ca2+-ATPase gene transfer reduces vascular smooth muscle cell proliferation and neointima formation in the rat // Circulat. Res. – 2005. – 97. – P. 488–95.
  73. Lipskaia L., Lompre A.Alteration in temporal kinetics of Ca2+ signaling and control of growth and prolifera- tion // Biol. Cell. – 2004. – 96. – P. 55–68.
  74. Ma Y., Hendershot L. The role of the unfolded protein response in tumour development: friend or foe? // Nat. Rev. Cancer. – 2004. – 4. – P. 966–977.
  75. Manning A., O’Brien N.,Kerin M. Roles for the calcium sensing receptor in primary and metastatic cancer // Eur. J. Surg. Oncol. – 2006. – 32. – P. 693–697.
  76. Mariot P., Vanoverberghe K., Lalevee N. et. al. Overexpression of an alpha 1H (Cav3.2) T-type calcium channel during neuroendocrine differentiation of human prostate cancer cells // J. Biol. Chem. – 2002. – 277. – P. 10824–10833.
  77. Marshall I., Burt R., Chapple C. Signal transduction pathways associated with alpha1-adrenoceptor sub- types in cells and tissues including human prostate // Eur. Urol. – 1999. – 36 Suppl 1. – P. 42–47; discussion 65.
  78. Mas-Oliva J., Perez-Montfort R., Cardenas-Garcia M., Rivas-Duro M. Altered coupling states between calcium transport and (Ca2+, Mg2+)-ATPase in the AS-30D as- cites hepatocarcinoma plasma membrane // Mol. Cell. Biochem. – 1991. – 100. – P. 39–50.
  79. 79. Mathiasen I., Sergeev I., Bastholm L. et. al. Calcium and calpain as key mediators of apoptosis-like death induced by vitamin D compounds in breast cancer cells // J. Biol. Chem. – 2002. – 277. – P. 30738–30745.
  80. 80. McConkey D., Lin Y., Nutt L. et. al. Cardiac glyco- sides stimulate Ca2+ increases and apoptosis in andro- gen-independent, metastatic human prostate adeno- carcinoma cells // Cancer. Res. – 2000. – 60. – P. 3807–3812.
  81. Mignen O., Brink C., Enfissi A. et. al. Carboxyami-mdotriazole-induced inhibition of mitochondrial calciummimport blocks capacitative calcium entry and cell pro-mliferation in HEK-293 cells // J. Cell. Sci. – 2005. –m118. P. 5615–5623.
  82. Msaouel P., Nixon A., Bramos A. et. al. Extracellularcalcium sensing receptor: an overview of physiology, pathophysiology and clinical perspectives // In Vivo. – 2004. – 18. – P. 739–753.
  83. Munaron L., Antoniotti S., Lovisolo D. Intracellular calcium signals and control of cell proliferation: how many mechanisms? // J. Cell. Mol. Med. – 2004. – 8. – P. 161–168.
  84. Murakami S. Hepatitis B virus X protein: a multifunc- tional viral regulator // J. Gastroenterol. – 2001. – 36. – P. 651–660.
  85. Nakagawa T., Zhu H., Morishima N. et. al. Caspase- 12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta // Nature. – 2000. – 403. – P. 98–103.
  86. Nicholson D. Caspase structure, proteolytic sub- strates, and function during apoptotic cell death // Cell. Death. Differ. – 1999. – 6. – P. 1028–1042.
  87. Nigg E. Cyclin-dependent protein kinases: key regulators of the eukaryotic cell cycle // Bioessays. – 1995. – 17. – P. 471–480.
  88. Nunez L., Valero R., Senovilla L. et. al. Cell prolifera- tion depends on mitochondrial Ca2+ uptake: inhibition by salicylate // J. Physiol. – 2006. – 571. – P. 57–73.
  89. 89. Okada Y., Maeno E. Apoptosis, cell volume regulation and volume–regulatory chloride channels // Comp. Biochem. Physiol. A Mol. Integr. Physiol. – 2001. – 130. – P. 377–383.
  90. 90. Okada Y., Shimizu T., Maeno E. et. al. Volume-sensi- tive chloride channels involved in apoptotic volume decrease and cell death // J. Membr. Biol. – 2006. – 209. – P. 21–29.
  91. 91. O’Rourke F., LaPlante J., Feinstein M. Antisense-me- diated loss of calcium homoeostasis endoplasmic reticulum protein (CHERP; ERPROT213-21) impairs Ca2+ mobilization, nuclear factor of activated T-cells (NFAT) activation and cell proliferation in Jurkat T- lymphocytes // Biochem. J. – 2003. – 373. – P. 133–143.
  92. 92. Orrenius S., Zhivotovsky B., Nicotera P. Regulation of cell death: the calcium-apoptosis link // Nat. Rev. Mol. Cell. Biol. – 2003. – 4. – P. 552–565.
  93. 93. Parekh A. Slow feedback inhibition of calcium release- activated calcium current by calcium entry // J. Biol. Chem. – 1998. – 273. – P. 14925–14932.
  94. 94. Patel M., Clunn G., Lymn J. et. al. Effect of serum withdrawal on the contribution of L-type calcium channels (CaV1.2) to intracellular Ca2+ responses and chemotaxis in cultured human vascular smooth muscle cells // Br. J. Pharmacol. – 2005. – 145. – P. 811–817.
  95. 95. Paterlini P., Driss F., Nalpas B. et. al. Persistence of hepa- titis B and hepatitis C viral genomes in primary liver cancers from HBsAg-negative patients: a study of a low- endemic area // Hepatology. – 1993. – 17. – P. 20–29.
  96. 96. Pawlotsky J. Pathophysiology of hepatitis C virus infection and related liver disease // Trends Microbiol. – 2004. – 12. – P. 96–102.
  97. 97. Peng J., Chen X., Berger U. et. al. Molecular cloning and characterization of a channel-like transporter medi- ating intestinal calcium absorption // J. Biol. Chem. – 1999. – 274. – P. 22739–22746.
  98. 98. Peng J., Zhuang L., Berger U. et. al. CaT1 expression correlates with tumor grade in prostate cancer // Biochem. and Biophys. Res. Commun. – 2001. – 282. – P. 729–734.
  99. 99. Pigozzi D., Ducret T., Tajeddine N. et. al. Calcium store contents control the expression of TRPC1, TRPC3 and TRPV6 proteins in LNCaP prostate cancer cell line // Cell. Calcium. – 2006. – 39. – P.401–415.
  100. 100. Pinton P., Ferrari D., Magalhaes P. et. al. Reduced loading of intracellular Ca2+ stores and downregulation of capacitative Ca2+ influx in Bcl-2-overexpressing cells // J. Cell. Biol. – 2000.– 148. – P. 857–862.
  101. 101. Prevarskaya N., Skryma R., Shuba Y. Ca2+ homeostasis in apoptotic resistance of prostate cancer cells // Biochem/ and Biophys. Res. Commun. – 2004. – 322. – P. 1326–1335.
  102. 102. Rao A., Luo C., Hogan P. Transcription factors of the NFAT family: regulation and function // Annu Rev Immunol .–1997.–15. – P. 707–747.
  103. 103. Rao R., Hermel E., Castro-Obregon S. et. al. Coupling endoplasmic reticulum stress to the cell death pro- gram. Mechanism of caspase activation // J. Biol. Chem. – 2001. –276. – P. 33869–33874.
  104. 104. Realdon S., Gerotto M., Dal Pero F. et. al. Proapop- totic effect of hepatitis C virus CORE protein in tran- siently transfected cells is enhanced by nuclear localization and is dependent on PKR activation // J. Hepatol. – 2004. – 40. – P. 77–85.
  105. 105. Reinhardt T., Filoteo A., Penniston J., Horst R. Ca(2+)-ATPase protein expression in mammary tis- sue // Amer. J. Physiol. Cell. Physiol. – 2000. – 279. – P. C1595–1602.
  106. 106. Reinhardt T., Horst R. Ca2+-ATPases and their ex- pression in the mammary gland of pregnant and lactating rats // Amer. J. Physiol. – 1999. – 276. – P. C796–802.
  107. 107. Reuter H., Pott C., Goldhaber J. et. al. Na+-Ca2+ ex- change in the regulation of cardiac excitation-contraction coupling // Cardiovasc. Res. –2005. – 67. – P. 198–207.
  108. 108. Rizzuto R., Bernardi P., Pozzan T. Mitochondria as all-round players of the calcium game // J. Physiol. – 2000. – 529 Pt 1. – P. 37–47.
  109. 109. Rizzuto R., Pinton P., Carrington W. et. al. Close contacts with the endoplasmic reticulum as determi- nants of mitochondrial Ca2+ responses // Science. – 1998. – 280. – P. 1763–1766.
  110. 110. Robertson J., Orrenius S., Zhivotovsky B. Review: nuclear events in apoptosis // J. Struct. Biol. – 2000. – 129. – P. 346–358.
  111. Rodland K. The role of the calcium-sensing receptor in cancer // Cell. Calcium. – 2004. – 35. – P. 291–295.
  112. Santella L. The role of calcium in the cell cycle: facts and hypotheses // Biochem. and Biophys. Res. Commun. – 1998. – 244. – P. 317–324.
  113. Savino J., 3rd Evans J., Rabinowitz D. et. al. Mul- tiple, disparate roles for calcium signaling in apoptosis of human prostate and cervical cancer cells exposed to diindolylmethane // Mol. Cancer. Therap. – 2006.–5. – P. 556–563.
  114. Schwarz E., Wissenbach U., Niemeyer B. et. al. TRPV6 potentiates calcium-dependent cell prolifera- tion // Cell. Calcium. – 2006. – 39. – P. 163–173.
  115. Sergeev I. Calcium signaling in cancer and vitamin D // J. Steroid. Biochem. Mol. Biol. – 2005. – 97. – P. 145–151.
  116. Shen M., Droogmans G., Eggermont J. et. al. Differ- ential expression of volume-regulated anion channels during cell cycle progression of human cervical cancer cells // J. Physiol. – 2000. – 529 Pt 2. – P. 385–394.
  117. Shen M., Yang T., Tang M. A novel function of BCL- 2 overexpression in regulatory volume decrease. Enhancing swelling-activated Ca2+ entry and Cl– channel activity // J. Biol. Chem. – 2002. – 277. – P. 15592–15599.
  118. Shimizu T., Morishima S., Okada Y. Ca2+-sensing receptor-mediated regulation of volume–sensitive Cl– channels in human epithelial cells // J. Physiol. – 2000. – 528. – P. 457–472.
  119. 119. Skryma R., Mariot P., Bourhis X. et. al. Store deple- tion and store-operated Ca2+ current in human pros- tate cancer LNCaP cells: involvement in apoptosis // J. Physiol. – 2000. – 527 Pt 1. – P. 71–83.
  120. 120. Smith L., Smith J. Regulation of sodium-calcium ex- changer by glucocorticoids and growth factors in vas- cular smooth muscle // J. Biol. Chem. – 1994. – 269. – P. 27527–27531.
  121. Strehler E., Zacharias D. Role of alternative splicing in generating isoform diversity among plasma membrane calcium pumps // Physiol. Rev. – 2001. – 81. – P. 21–50.
  122. Sweeney M., Yu Y., Platoshyn O. et. al. Inhibition of endogenous TRP1 decreases capacitative Ca2+ entry and attenuates pulmonary artery smooth muscle cell proliferation // Amer. J. Physiol. Lung. Cell. Mol. Physiol. – 2002. –283. – P. L144–155.
  123. Sweet S., Singh G. Changes in mitochondrial mass, membrane potential, and cellular adenosine triphosphate content during the cell cycle of human leukemic (HL-60) cells // J. Cell. Physiol. – 1999. – 180. – P. 91–96.
  124. Tfelt-Hansen J., Ferreira A., Yano S., Kanuparthi D. Calcium–sensing receptor activation induces nitric oxide production in H-500 Leydig cancer cells // Amer. J. Physiol. Endocrinol. Metab. – 2005. – 288. – P. E1206–1213.
  125. Thebault S., Flourakis M., Vanoverberghe K. et. al. Differential role of transient receptor potential channels in Ca2+ entry and proliferation of prostate cancer epithelial cells // Cancer. Res. – 2006. – 66. – P. 2038–2047.
  126. Thebault S., Roudbaraki M., Sydorenko V. et.al. Al- pha1-adrenergic receptors activate Ca2+-permeable cationic channels in prostate cancer epithelial cells // J. Clin. Invest. – 2003. – 111. – P. 1691–1701.
  127. Thomas A., Bird G., Hajnoczky G., Robb-Gaspers L. Spatial and temporal aspects of cellular calcium signal- ing // Faseb. J. – 1996. – 10. – P. 1505–1517.
  128. Vallot O., Combettes L., Jourdon P. et. al. Intracellu- lar Ca2+ handling in vascular smooth muscle cells is affected by proliferation // Arterioscler. Thromb. Vas- cular. Biol. – 2000. – 20. – P. 1225–1235.
  129. 129. Van de Craen M., Vandenabeele P., Declercq W. et. al. Characterization of seven murine caspase family members // FEBS Lett. – 1997.– 403. – P. 61–69.
  130. 130. Vanden Abeele F., Lemonnier L., Thebault S. et.al. Two types of store–operated Ca2+ channels with dif- ferent activation modes and molecular origin in LNCaP human prostate cancer epithelial cells // J. Biol. Chem. – 2004. – 279. – P. 30326–30337.
  131. Vanden Abeele F., Roudbaraki M., Shuba Y. et al. Store-operated Ca2+ current in prostate cancer epithe- lial cells. Role of endogenous Ca2+ transporter type 1 // J. Biol. Chem. – 2003. – 278. – P. 15381–15389.
  132. Vanden Abeele F., Skryma R., Shuba Y. et. al. Bcl-2- dependent modulation of Ca2+ homeostasis and store- operated channels in prostate cancer cells // Cancer. Cell. – 2002. – 1. – P. 169–179.
  133. Vanoverberghe K., Mariot P., Vanden Abeele F. et. al. Mechanisms of ATP–induced calcium signaling and growth arrest in human prostate cancer cells // Cell. Calcium. – 2003. – 34. – P. 75–85.
  134. Vanoverberghe K., Vanden Abeele F., Mariot P. et. al. Ca2+ homeostasis and apoptotic resistance of neuroendocrine-differentiated prostate cancer cells // Cell. Death. Differ. – 2004. – 11. – P. 321–330.
  135. Varadi A., Cirulli V., Rutter G. Mitochondrial localization as a determinant of capacitative Ca2+ en- try in HeLa cells // Cell. Calcium. – 2004.– 36. – P. 499–508.
  136. Von Kugelgen I., Wetter A. Molecular pharmacology of P2Y-receptors // Naunyn Schmiedebergs Arch. Pharmacol. – 2000. – 362. – P. 310–323.
  137. Waldron R., Short A., Meadows J. et al. Endoplasmic reticulum calcium pump expression and control of cell growth // J. Biol. Chem. – 1994.– 269. – P. 11927–11933.
  138. Wang H., Pathan N., Ethell I. et. al. Ca2+-induced apoptosis through calcineurin dephosphorylation of BAD // Science. – 1999. – 284. – P. 339–343.
  139. 139. Wang L., Chen L., Zhu L., Rawle M. Regulatory volume decrease is actively modulated during the cell cycle // J. Cell. Physiol. – 2002. – 193. – P. 110–119.
  140. 140. Wang X., Nagaba Y., Cross H. et. al. The mRNA of L- type calcium channel elevated in colon cancer: protein distribution in normal and cancerous colon // Amer. J. Pathol. – 2000. – 157. – P. 1549–1562.
  141. Williams S., French J., Gilbert M. et. al. Bcl-2 overexpression results in enhanced capacitative calcium entry and resistance to SKF-96365-induced apoptosis // Cancer. Res. – 2000. – 60. – P. 4358–4361.
  142. Wissenbach U., Niemeyer B., Fixemer T. et. al. Ex- pression of CaT-like, a novel calcium-selective channel, correlates with the malignancy of prostate cancer // J. Biol. Chem. – 2001. – 276. – P. 19461–19468.
  143. Yu Y., Fantozzi I., Remillard C. et. al. Enhanced ex- pression of transient receptor potential channels in idiopathic pulmonary arterial hypertension // Proc. Natl. Acad. Sci. USA. – 2004. – 101. – P. 13861–13866.
  144. Yu Y., Sweeney M., Zhang S. et. al. PDGF stimu- lates pulmonary vascular smooth muscle cell prolif- eration by upregulating TRPC6 expression // Amer. J. Physiol. Cell. Physiol. – 2003. – 284. – P. C316–330.
  145. Yue L., Peng J., Hediger M., Clapham D. CaT1 mani- fests the pore properties of the calcium-release-activated calcium channel // Nature. – 2001.– 410. – P. 705–709.
  146. Zhuang L., Peng J., Tou L. et. al. Calcium-selective ion channel, CaT1, is apically localized in gastrointes- tinal tract epithelia and is aberrantly expressed in human malignancies // Lab. Invest. – 2002. – 82. – P. 1755–1764.

© National Academy of Sciences of Ukraine, Bogomoletz Institute of Physiology, 2014-2024.