Endoplasmic reticulum calcium pumps and cancer

BioFactors

Volumn 37, Issue 3, 2011, Pages 139-149

  Arbabian, Atousa ^a   Brouland, Jean Philippe ^b   Gélébart, Pascal ^c   Kovàcs, Tünde ^d   Bobe, Régis ^e   Enouf, Jocelyne ^b   Papp, Béla ^a  

^a INSERM   (France)

^b HÔPITAL LARIBOISIÈRE   (France)

^c UNIVERSITY OF ALBERTA   (Canada)

^d SEMMELWEIS UNIVERSITY   (Hungary)

^e Dept Environ Med Natl Inst Publ HIth   (Norway)

Author keywords

Calcium; Cancer; Differentiation; Endoplasmic reticulum; SERCA

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); ADENOSINE TRIPHOSPHATASE (CALCIUM) 2; ADENOSINE TRIPHOSPHATASE (CALCIUM) 3; BETA CATENIN; CALCIUM; INTERLEUKIN 2; PROTEIN ZO1; RETINOIC ACID; RETINOIC ACID RECEPTOR ALPHA; THAPSIGARGIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RARALPHA; UNCLASSIFIED DRUG;

CALCIUM BINDING; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CALCIUM TRANSPORT; CARCINOGENESIS; CELL DIFFERENTIATION; COLON CARCINOMA; DOWN REGULATION; DRUG MECHANISM; DRUG TARGETING; ENDOPLASMIC RETICULUM; GENE EXPRESSION; GENE MUTATION; HEART MUSCLE CELL; HUMAN; IMMUNOHISTOCHEMISTRY; LYMPHOCYTE ACTIVATION; NEOPLASM; PRIORITY JOURNAL; PROMYELOCYTIC LEUKEMIA; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

EID: 79959527283     PISSN: 09516433     EISSN: 18728081     Source Type: Journal    
DOI: 10.1002/biof.142     Document Type: Review

References (144)

1. Berridge, M.J. (2004) Calcium signal transduction and cellular control mechanisms. Biochim. Biophys. Acta. 1742, 3-7.
2. Berridge, M.J., Lipp P., and Bootman, M.D. (2000) The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell. Biol. 1, 11-21.
3. Berridge, M.J. (2006) Calcium microdomains: organization and function. Cell Calcium 40, 405-412.
4. Berridge, M.J. (2007) Inositol trisphosphate and calcium oscillations. Biochem. Soc. Symp. 74, 1-7.
5. Berridge, M.J. (2009) Inositol trisphosphate and calcium signalling mechanisms. Biochim. Biophys. Acta. 1793, 933-940.
6. 2+ response amplitude and duration. Nature 386, 855-858.
7. Dolmetsch, R.E., Xu, K., and Lewis, R.S. (1998) Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392, 933-936.
8. Lewis, R.S. (2003) Calcium oscillations in T-cells: mechanisms and consequences for gene expression. Biochem. Soc. Trans. 31, 925-929.
9. Macian, F., Lopez-Rodriguez, C., and Rao, A. (2001) Partners in transcription: NFAT and AP-1. Oncogene 20, 2476-2489.
10. Kaufman, R.J. (1999) Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev. 13, 1211-1233.
11. Brostrom, M.A. and Brostrom, C.O. (2003) Calcium dynamics and endoplasmic reticular function in the regulation of protein synthesis: implications for cell growth and adaptability. Cell Calcium 34, 345-363.
12. Ni, M. and Lee A.S. (2007) ER chaperones in mammalian development and human diseases. FEBS Lett. 581, 3641-3651.
13. Otsu, M. and Sitia, R. (2007) Diseases originating from altered protein quality control in the endoplasmic reticulum. Curr. Med. Chem. 14, 1639-1652.
14. Ruddock, L.W. and Molinari, M. (2006) N-glycan processing in ER quality control. J Cell Sci. 119, 4373-4380.
15. 2+ signaling and calcium binding chaperones of the endoplasmic reticulum. Cell Calcium 32, 269-278.
16. Rao, R.V., Ellerby, H.M., and Bredesen, D.E. (2004) Coupling endoplasmic reticulum stress to the cell death program. Cell. Death. Differ. 11, 372-380.
17. Ron, D. and Walter, P. (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell. Biol. 8, 519-529.
18. Pelletier, N., Casamayor-Palleja, M., De Luca, K., Mondière, P., Saltel, F., Jurdic, P., Bella, C., Genestier, L., and Defrance, T. (2006) The endoplasmic reticulum is a key component of the plasma cell death pathway. J. Immunol. 176, 1340-1347.
19. Putney, J.W., Jr. (2007) Recent breakthroughs in the molecular mechanism of capacitative calcium entry (with thoughts on how we got here). Cell Calcium 42, 103-110.
20. Hovnanian, A. (2007) SERCA pumps and human diseases. Subcell. Biochem. 45, 337-363.
21. Dally, S., Corvazier, E., Bredoux, R., Bobe, R., and Enouf, J. (2010) Multiple and diverse coexpression, location, and regulation of additional SERCA2 and SERCA3 isoforms in nonfailing and failing human heart. J. Mol. Cell. Cardiol. 48, 633-644.
22. Feske, S. (2007) Calcium signalling in lymphocyte activation and disease. Nat. Rev. Immunol. 7, 690-702.
23. 2+ pool. Cell Calcium 48, 143-149.
24. Periasamy, M. and Kalyanasundaram, A. (2007) SERCA pump isoforms: their role in calcium transport and disease. Muscle Nerve 35, 430-442.
25. Prasad, V., Okunade, G.W., Miller, M.L., and Shull, G.E. (2004) Phenotypes of SERCA and PMCA knockout mice. Biochem. Biophys. Res. Commun. 322, 1192-1203.
26. 2+ storage in health and disease: a dynamic equilibrium. Cell Calcium 47, 297-314.
27. Wuytack, F., Raeymaekers, L., and Missiaen, L. (2002) Molecular physiology of the SERCA and SPCA pumps. Cell Calcium 32, 279-305.
28. Berridge, M.J. (2002) The endoplasmic reticulum: a multifunctional signaling organelle. Cell Calcium 32, 235-249.
29. Diederichs, F. (2008) Ion homeostasis and the functional roles of SERCA reactions in stimulus-secretion coupling of the pancreatic beta-cell: A mathematical simulation. Biophys. Chem. 134, 119-143.
30. Szabadkai, G. and Rizzuto, R. (2007) Chaperones as parts of organelle networks. Adv. Exp. Med. Biol. 594, 64-77.
31. Zhang, K. and Kaufman, R.J. (2006) The unfolded protein response: a stress signaling pathway critical for health and disease. Neurology 66, S102-109.
32. Cahalan, M.D., Zhang, S.L., Yeromin, A.V., Ohlsen, K., Roos, J., and Stauderman, K.A. (2007) Molecular basis of the CRAC channel. Cell Calcium 42, 133-144.
33. Johnstone, L.S., Graham, S.J., and Dziadek, M.A. (2010) STIM proteins: integrators of signalling pathways in development, differentiation and disease. J. Cell. Mol. Med. 14, 1890-1903.
34. Brini, M. and Carafoli, E. (2009) Calcium pumps in health and disease. Physiol. Rev. 89, 1341-1378.
35. Monteith, G.R., McAndrew, D., Faddy, H.M., and Roberts-Thomson, S.J. (2007) Calcium and cancer: targeting Ca2+ transport. Nat. Rev. Cancer 7, 519-530.
36. 2+-store in cancer. Anticancer. Agents. Med. Chem. 8, 705-709.
37. 2+ for cancer cell proliferation and survival. Nat. Rev. Cancer 8, 361-375.
38. Parkash, J. and Asotra, K. (2010) Calcium wave signaling in cancer cells. Life Sci. 87, 587-595
39. Barr, V.A., Bernot, K.M., Shaffer, M.H., Burkhardt, J.K., and Samelson, L.E. (2009) Formation of STIM and Orai complexes: puncta and distal caps. Immunol. Rev. 231, 148-159.
40. 2+ entry. Nat. Cell. Biol. 11, 669-677.
41. Putney, J.W. (2009) Capacitative calcium entry: from concept to molecules. Immunol. Rev. 231, 10-22.
42. Hogan, P.G., Lewis, R.S., and Rao, A. (2010) Molecular basis of calcium signaling in lymphocytes: STIM and ORAI. Annu. Rev. Immunol. 28, 491-533.
43. Landgraf, G., Gellerich, F.N., and Wussling, M.H. (2004) Inhibitors of SERCA and mitochondrial Ca-uniporter decrease velocity of calcium waves in rat cardiomyocytes. Mol. Cell. Biochem. 256-257, 379-386.
44. 2+ ATPase (SERCA) inhibition. J. Bioenerg. Biomembr. 37, 365-368.
45. 2+ stores in smooth muscle cells. Am. J. Physiol. Cell. Physiol. 298, C1038-1046.
46. 2+ (SERCA)-pumps: link to heart beats and calcium waves. Cell Calcium 25, 277-290.
47. Higgins, E.R., Cannell M.B., and Sneyd J. (2006) A buffering SERCA pump in models of calcium dynamics. Biophys. J. 91, 151-163.
48. Juska, A. (2006) Dynamics of calcium fluxes in nonexcitable cells: mathematical modeling. J. Membr. Biol. 211, 89-99.
49. 2+ uptake by the endoplasmic reticulum. J. Theor. Biol. 237, 279-290.
50. Kauffman, K.J., Pridgen, E.M., Doyle, F.J. III, Dhurjati, P.S., and Robinson, A.S. (2002) Decreased protein expression and intermittent recoveries in BiP levels result from cellular stress during heterologous protein expression in Saccharomyces cerevisiae. Biotechnol. Prog. 18, 942-950.
51. Buchberger, A., Bukau, B., and Sommer, T. Protein quality control in the cytosol and the endoplasmic reticulum: brothers in arms. Mol. Cell. 40, 238-252.
52. Bànhegyi, G., Baumeister, P., Benedetti, A., Dong, D., Fu, Y., Lee, A.S., Li, J., Mao, C., Margittai, E., Ni, M., Paschen, W., Piccirella, S., Senesi, S., Sitia, R., Wang, M., and Yang, W. (2007) Endoplasmic reticulum stress. Ann. NY Acad. Sci. 1113, 58-71.
53. 2+ pump isoforms 1, 2, and 3 to thapsigargin and other inhibitors. J. Biol. Chem. 281, 6970-6976.
54. Hakii, H., Fujiki, H., Suganuma, M., Nakayasu, M., Tahira, T., Sugimura, T., Scheuer, P.J., and Christensen, S.B. (1986) Thapsigargin, a histamine secretagogue, is a non-12-O-tetradecanoylphorbol-13-acetate (TPA) type tumor promoter in two-stage mouse skin carcinogenesis. J. Cancer Res. Clin. Oncol. 111, 177-181.
55. Sakai, A. and Teshima, R. (2001) 2, 5-Di-tert-butyl-1, 4-hydroquinone enhances cell transformation accompanied by an increase in intracellular free calcium ion concentration. Cancer Lett. 168, 183-190.
56. Korosec, B., Glavac, D., Rott, T., and Ravnik-Glavac, M. (2006) Alterations in the ATP2A2 gene in correlation with colon and lung cancer. Cancer Genet. Cytogenet. 171, 105-111.
57. 2+ pumps in association with head and neck squamous cell carcinoma. Cancer Genet. Cytogenet. 181, 112-118.
58. Korosec, B., Glavac, D., Volavsek, M., and Ravnik-Glavac, M. (2009) ATP2A3 gene is involved in cancer susceptibility. Cancer Genet. Cytogenet. 188, 88-94.
59. 2+ ATPase type 2 downregulated in human oral squamous cell carcinoma. Int. J. Cancer 110, 225-231.
60. 2+-ATPases in thyroid and its down-regulation following neoplastic transformation. J. Mol. Endocrinol. 30, 399-409.
61. 2+-homeostasis is altered in Small and non-small Cell Lung Cancer cell lines. J. Exp. Clin. Cancer Res. 28, 25.
62. Chung, F.Y., Lin, S.R., Lu, C.Y., Yeh, C.S., Chen, F.M., Hsieh, J.S., Huang, T.J., and Wang, JY. (2006) Sarco/endoplasmic reticulum calcium-ATPase 2 expression as a tumor marker in colorectal cancer. Am. J. Surg. Pathol. 30, 969-974.
63. Takahashi, M., Kondou, Y., and Toyoshima, C. (2007) Interdomain communication in calcium pump as revealed in the crystal structures with transmembrane inhibitors. Proc. Natl. Acad. Sci. U S A. 104, 5800-5805.
64. Toyoshima, C. (2007) Ion pumping by calcium ATPase of sarcoplasmic reticulum. Adv. Exp. Med. Biol. 592, 295-303.
65. Toyoshima, C. and Mizutani, T. (2004) Crystal structure of the calcium pump with a bound ATP analogue. Nature 430, 529-535.
66. Toyoshima, C., Nakasako, M., Nomura, H., and Ogawa, H. (2000) Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 Å resolution. Nature 405, 647-655.
67. Toyoshima, C., Norimatsu, Y., Iwasawa, S., Tsuda, T., and Ogawa, H. (2007) How processing of aspartylphosphate is coupled to lumenal gating of the ion pathway in the calcium pump. Proc. Natl. Acad. Sci. U S A. 104, 19831-19836.
68. 2+-ATPase: design of a perfect chemi-osmotic pump. Q. Rev. Biophys. 1-66.
69. 2+-ATPase pumps ions across the sarcoplasmic reticulum membrane. Biochim. Biophys. Acta 1793, 94194-94196.
70. Gélébart, P., Martin, V., Enouf, J., and Papp, B. (2003) Identification of a new SERCA2 splice variant regulated during monocytic differentiation. Biochem. Biophys. Res. Commun. 303, 676-684.
71. Sakuntabhai, A., Ruiz-Perez, V., Carter, S., Jacobsen, N., Burge, S., Monk, S., Smith, M., Munro, C.S., O'Donovan, M., Craddock, N., Kucherlapati, R., Rees, J.L., Owen, M., Lathrop, G.M., Monaco, A.P., Strachan, T., and Hovnanian, A. (1999) Mutations in ATP2A2, encoding a Ca2+ pump, cause Darier disease. Nat. Genet. 21, 271-277.
72. 2+ pump. J. Biol. Chem. 276, 26737-26740.
73. 2+ homeostasis in pancreatic beta-cells. Diabetes 51, 3245-3253.
74. Kao, J., Fortner, C.N., Liu, L.H., Shull, G.E., and Paul, R.J. (1999) Ablation of the SERCA3 gene alters epithelium-dependent relaxation in mouse tracheal smooth muscle. Am. J. Physiol. 277, L264-270.
75. 2+ ATPase (SERCA) 3 proteins in two major conformational states in native human cell membranes. Biochim. Biophys. Acta 1788, 587-599.
76. 2+-ATPase isoforms are expressed in a cell type? A growing family of membrane proteins illustrated by studies in platelets. Platelets 16, 133-150.
77. 2+-ATPase (SERCA) 3 isoforms. Expression, regulation, and function of the membranes of the SERCA3 family. J. Biol. Chem. 277, 24442-24452.
78. 2+-ATPase isoform transcripts. Am. J. Physiol. 269, C775-784.
79. 2+ pumps. Biosci. Rep. 15, 299-306.
80. Poch, E., Leach, S., Snape, S., Cacic, T., MacLennan, D.H., and Lytton, J. (1998) Functional characterization of alternatively spliced human SERCA3 transcripts. Am. J. Physiol. 275, C1449-1458.
81. Ozog, A., Pouzet, B., Bobe, R., and Lompré, A.-M. (1998) Characterization of the 3' end of the mouse SERCA 3 gene and tissue distribution of mRNA spliced variants. FEBS Lett. 427, 349-352.
82. 2+ pumps in the brain. Mol. Chem. Neuropathol. 33, 199-208.
83. 2+-ATPase isoforms during ontogeny in the rat. J. Mol. Cell. Cardiol. 26, 539-550.
84. 2+-ATPase mRNA isoform, SERCA 3, is expressed in endothelial and epithelial cells in various organs. FEBS Lett. 334, 45-48.
85. 2+-ATPase type 3 gene in endothelial cells is controlled by Ets-1 and Sp1. J. Biol. Chem. 277, 36471-36478.
86. Lytton, J., Westlin, M., Burk, S.E., Shull, G.E., and MacLennan, D.H. (1992) Functional comparisons between isoforms of the sarcoplasmic or endoplasmic reticulum family of calcium pumps. J. Biol. Chem. 267, 14483-14489.
87. 2+ transport (SERCA) ATPase. Biochemistry 39, 8758-8767.
88. Strehler, E.E. and Treiman, M. (2004) Calcium pumps of plasma membrane and cell interior. Curr. Mol. Med. 4, 323-335.
89. 2+ oscillations in pancreatic islets. Bull. Math. Biol. 70, 1251-1271.
90. 2+-ATPase (SERCA) 1 and 3 isoforms by steady-state and transient kinetic analyses. J. Biol. Chem. 277, 45579-45591.
91. Chandrasekera, P.C., Kargacin, M.E., Deans, J.P., and Lytton, J. (2009) Determination of apparent calcium affinity for endogenously expressed human sarco(endo)plasmic reticulum calcium-ATPase isoform SERCA3. Am. J. Physiol. Cell. Physiol. 296, C1105-1114.
92. 2+-ATPases. J. Biol. Chem. 267, 14490-14496.
93. 2+-ATPase of the endoplasmic reticulum. Am. J. Physiol. Cell. Physiol. 290, C1503-1511.
94. Juska, A., Jardin, I., and Rosado, J.A. (2008) Physical properties of two types of calcium stores and SERCAs in human platelets. Mol. Cell. Biochem. 311, 9-18.
95. Smith-Garvin, J.E., Koretzky, G.A., and Jordan, M.S. (2009) T cell activation. Annu. Rev. Immunol. 27, 591-619.
96. Liu, J.O. (2009) Calmodulin-dependent phosphatase, kinases, and transcriptional corepressors involved in T-cell activation. Immunol Rev, 228, 184-198.
97. Launay, S., Bobe, R., Lacabaratz-Porret, C., Bredoux, R., Kovàcs, T., Enouf, J., and Papp, B. (1997) Modulation of endoplasmic reticulum calcium pump expression during T lymphocyte activation. J. Biol. Chem. 272, 10746-10750.
98. Dellis, O., Arbabian, A., Brouland, J-P., Kovàcs, T, Rowe, M., Chomienne, C., Joab, I., and Papp, B. (2009) Modulation of B-cell endoplasmic reticulum calcium homeostasis by Epstein-Barr virus latent membrane protein-1. Mol. Cancer 8, 59.
99. Dugas, B., Delfraissy, J.F., Calenda, A., Peuchmaur, M., Wallon, C., Rannou, M.T., and Galanaud, P. (1988) Activation and infection of B cells by Epstein-Barr virus. Role of calcium mobilization and of protein kinase C translocation. J. Immunol. 141, 4344-4351.
100. Farrell, P.J., Cludts, I., and Stuhler, A. (1997) Epstein-Barr virus genes and cancer cells. Biomed. Pharmacother. 51, 258-267.
101. Swerdlow, S.H. (2008) International Agency for Research on Cancer., World Health Organization. WHO classification of tumours of haematopoietic and lymphoid tissues. International Agency for Research on Cancer, Lyon, France.
102. Farrell, P.J. (1998) Signal transduction from the Epstein-Barr virus LMP-1 transforming protein. Trends Microbiol. 6, 175-7; discussion 177-178.
103. Klein, E., Teramoto, N., Gogolak, P., Nagy, N., and Bjorkholm, M. (1999) LMP-1, the Epstein-Barr virus-encoded oncogene with a B cell activating mechanism similar to CD40. Immunol. Lett. 68, 147-54.
104. Pinto, D. and Clevers, H. (2005) Wnt, stem cells and cancer in the intestine. Biol. Cell. 97, 185-196.
105. Kountouras, J., Boura, P., and Lygidakis, N.J. (2000) New concepts of molecular biology for colon carcinogenesis. Hepatogastroenterology 47, 1291-1297.
106. Bright-Thomas, R.M. and Hargest, R. (2003) APC, beta-Catenin and hTCF-4; an unholy trinity in the genesis of colorectal cancer. Eur. J. Surg. Oncol. 29, 107-117.
107. Artursson, P. (1990) Epithelial transport of drugs in cell culture. I: A model for studying the passive diffusion of drugs over intestinal absorptive (Caco-2) cells. J. Pharm. Sci. 79, 476-482.
108. Brouland, J.P., Gélébart, P., Kovàcs, T., Enouf, J., Grossmann, J., and Papp, B. (2005) The loss of sarco/endoplasmic reticulum calcium transport ATPase 3 expression is an early event during the multistep process of colon carcinogenesis. Am. J. Pathol. 167, 233-242.
109. Gélébart, P., Kovàcs, T., Brouland, J.-P., van Gorp, R., Grossmann, J., Rivard, N., Panis, Y., Martin, V., Bredoux, R., Enouf, J., and Papp, B. (2002) Expression of endomembrane calcium pumps in colon and gastric cancer cells. Induction of SERCA3 expression during differentiation. J. Biol. Chem. 277, 26310-26320.
110. Aaltonen, L.A. and Hamilton, S.R., (2000) World Health Organization., International Agency for Research on Cancer. Pathology and genetics of tumours of the digestive system. IARC Press, Lyon, Oxford.
111. Kikuchi, Y., Dinjens, W.N., and Bosman, F.T. (1997) Proliferation and apoptosis in proliferative lesions of the colon and rectum. Virchows Arch. 431, 111-117.
112. Tateyama, H., Li, W., Takahashi, E., Miura, Y., Sugiura, H., and Eimoto, T. (2002) Apoptosis index and apoptosis-related antigen expression in serrated adenoma of the colorectum: the saw-toothed structure may be related to inhibition of apoptosis. Am. J. Surg. Pathol. 26, 249-256.
113. 2+-ATPase expression during colon and gastric cancer cell differentiation. Cell Calcium 42, 590-605.
114. 2+-ATPase expression during colon cancer cell line differentiation. Biochem. Biophys. Res. Commun. 355, 932-936.
115. Aung, C.S., Ye, W., Plowman, G., Peters, A.A., Monteith, G.R., and Roberts-Thomson, S.J. (2009) Plasma membrane calcium ATPase 4 and the remodeling of calcium homeostasis in human colon cancer cells. Carcinogenesis 30, 1962-1969.
116. Chomienne, C., Fenaux, P., and Degos, L. (1996) Retinoid differentiation therapy in promyelocytic leukemia. FASEB J. 10, 1025-1030.
117. Nasr, R., Guillemin, M.-C., Ferhi, O., Soilihi, H., Peres, L., Berthier, C., Rousselot, P., Robledo-Sarmiento, M., Lallemand-Breitenbach, V., Gourmel, B., Vitoux, D., Pandolfi, P.P., Rochette-Egly, C., Zhu, J., and de Thé, H. (2008) Eradication of acute promyelocytic leukemia-initiating cells through PML-RARA degradation. Nat. Med. 14, 1333-1342.
118. Launay, S., Giannì, M., Kovàcs, T., Bredoux, R., Bruel, A., Gélébart, P., Zassadowski, F., Chomienne, C., Enouf, J., and Papp, B. (1999) Lineage-specific modulation of calcium pump expression during myeloid differentiation. Blood 93, 4395-4405.
119. Guillemin, M.-C., Raffoux, E., Vitoux, D., Kogan, S., Soilihi, H., Lallemand-Breitenbach, V., Zhu, J., Janin, A., Daniel, M.T., Gourmel, B., Degos, L., Dombret, H., Lanotte, M., and De Thé, H. (2002) In vivo activation of cAMP signaling induces growth arrest and differentiation in acute promyelocytic leukemia. J. Exp. Med. 196, 1373-1380.
120. Zhao, Q., Tao, J., Zhu, Q., Jia, P.M., Dou, A.X., Li, X., Cheng, F., Waxman, S., Chen, G.Q., Chen, S.J., Lanotte, M., Chen, Z., and Tong, J.H. (2004) Rapid induction of cAMP/PKA pathway during retinoic acid-induced acute promyelocytic leukemia cell differentiation. Leukemia 18, 285-292.
121. Vintermyr, O.K., Gjertsen, B.T., Lanotte, M., and Doskeland, S.O. (1993) Microinjected catalytic subunit of cAMP-dependent protein kinase induces apoptosis in myeloid leukemia (IPC-81) cells. Exp. Cell. Res. 206, 157-161.
122. 2+ signalling during megakaryocytic differentiation: an in vitro study. Biochem. J. 350 Pt 3, 723-734.
123. Papp, B., Pàszty, K., Kovàcs, T., Sarkadi, B., Gàrdos, G., Enouf, J., and Enyedi, A. (1993) Characterization of the inositol trisphosphate-sensitive and insensitive calcium stores by selective inhibition of the endoplasmic reticulum-type calcium pump isoforms in isolated platelet membrane vesicles. Cell Calcium 14, 531-538.
124. Jardin, I., Lopez, J.J., Pariente, J.A., Salido, G.M., and Rosado, J.A. (2008) Intracellular calcium release from human platelets: different messengers for multiple stores. Trends. Cardiovasc. Med. 18, 57-61.
125. 2+ store refilling by interaction with SERCA3 in human platelets. Biochem. Pharmacol. 75, 2157-2164.
126. 2+ stores in sarcoplasmic and endoplasmic reticulum. Science 275, 1643-1648.
127. 2+] subcompartments in intact HeLa cells. J. Cell Biol. 139, 601-611.
128. 2+] microdomains control agonist-induced Ca2+ release in intact HeLa cells. FASEB J. 11, 881-885.
129. 2+ signaling in polarized exocrine cells. Adv. Exp. Med. Biol. 506, 175-183.
130. Kiselyov, K., Wang, X., Shin, D.M., Zang, W., and Muallem, S. (2006) Calcium signaling complexes in microdomains of polarized secretory cells. Cell Calcium 40, 451-459.
131. 2+]i waves. J. Biol. Chem. 272, 15771-15776.
132. Orci, L., Ravazzola, M., Le Coadic, M., Shen, W.W., Demaurex, N., and Cosson, P. (2009) STIM1-induced precortical and cortical subdomains of the endoplasmic reticulum. Proc. Natl. Acad. Sci. U S A 106, 19358-19362.
133. 2+-ATPases. Trends Pharmacol. Sci. 19, 131-135.
134. Papp, B and Byrn, R.A. (1995) Stimulation of HIV expression by intracellular calcium pump inhibition. J. Biol. Chem. 270, 10278-10283.
135. Sei, Y and Reich, H. (1995) Thapsigargin induces IL-2 receptor alpha-chain in human peripheral and Jurkat T cells via a protein kinase C-independent mechanism. Immunol. Lett. 45, 75-80.
136. Apàti, A, Jànossy, J, Bròzik, A, Bauer, P.I., and Magòcsi, M. (2003) Calcium induces cell survival and proliferation through the activation of the MAPK pathway in a human hormone-dependent leukemia cell line, TF-1. J. Biol. Chem. 278, 9235-9243.
137. Apàti, A, Jànossy, J., Bròzik, A., and Magòcsi, M. (2003) Effects of intracellular calcium on cell survival and the MAPK pathway in a human hormone-dependent leukemia cell line (TF-1). Ann. N Y. Acad. Sci. 1010, 70-73.
138. Launay, S., Giannì, M., Diomede, L., Machesky, L.M., Enouf, J., and Papp, B. (2003) Enhancement of ATRA-induced cell differentiation by inhibition of calcium accumulation into the endoplasmic reticulum: cross-talk between RAR alpha and calcium-dependent signaling. Blood 101, 3220-3228.
139. 2+-ATPases 2B involvement in human prostate cancer cell growth control. J. Biol. Chem. 276, 47608-47614.
140. Gong, Y., Blok, L.J., Perry, J.E., Lindzey, J.K., and Tindall, D.J. (1995) Calcium regulation of androgen receptor expression in the human prostate cancer cell line LNCaP. Endocrinology 136, 2172-2178.
141. Christensen, S.B., Skytte, D.M., Denmeade, S.R., Dionne, C., Møller, J.V., Nissen, P., and Isaacs, J.T. (2009) A Trojan horse in drug development: targeting of thapsigargins towards prostate cancer cells. Anticancer Agents Med. Chem. 9, 276-294.
142. Denmeade, S.R. and Isaacs, J.T. (2005) The SERCA pump as a therapeutic target: making a "smart bomb" for prostate cancer. Cancer Biol. Ther. 4, 14-22.
143. O'Neill, J.P., Velalar, C.N., Lee, D.I., Zhang, B., Nakanishi, T., Tang, Y., Selaru, F., Ross, D., Meltzer, S.J., and Hussain, A. (2006) Thapsigargin resistance in human prostate cancer cells. Cancer 107, 649-659.
144. Identifier: NCT01056029, Available at: Accessed on January 18, 2011