Vitamin D3regulates the formation and degradation of gap junctions in androgen-responsive human prostate cancer cells

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Kelsey, Linda ^a   Katoch, Parul ^a   Ray, Anuttoma ^a   Mitra, Shalini ^a   Chakraborty, Souvik ^a   Lin, Ming Fong ^a   Mehta, Parmender P ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; CALCITRIOL; CONNEXIN 32; COLECALCIFEROL; GAP JUNCTION PROTEIN; RETINOID;

ARTICLE; CANCER INHIBITION; CELL MIGRATION; CELL STRUCTURE; CONTROLLED STUDY; GAP JUNCTION; HUMAN; HUMAN CELL; LNCAP CELL LINE; MALE; NERVE CELL DIFFERENTIATION; PROSTATE CANCER; PROSTATE TUMOR; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; ANIMAL; DRUG EFFECTS; METABOLISM; TUMOR CELL LINE; WESTERN BLOTTING;

ANDROGENS; ANIMALS; BLOTTING, WESTERN; CELL LINE, TUMOR; CHOLECALCIFEROL; CONNEXINS; GAP JUNCTIONS; HUMANS; MALE; PROSTATIC NEOPLASMS; RECEPTORS, ANDROGEN; RETINOIDS;

EID: 84906959438     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0106437     Document Type: Article

References (93)

1. Fleet JC, Desmet M, Johnson R, Li Y (2012) Vitamin D and cancer: a review of molecular mechanisms. Biochemical Journal 441: 61-76.
2. Deeb KK, Trump DL, Johnson CS (2007) Vitamin D signalling pathways in cancer: potential for anticancer therapeutics. Nat Rev Cancer 7: 684-700.
3. Swami S, Krishnan AV, Feldman D (2011) Vitamin D metabolism and action in the prostate: Implications for health and disease. Molecular and Cellular Endocrinology 347: 61-69.
4. Krishnan AV, Feldman D (2010) Molecular pathways mediating the anti-inflammatory effects of calcitriol: implications for prostate cancer chemoprevention and treatment. Endocr Relat Cancer 17: R19-R38.
5. Schwartz GG, Hulka BS (1990) Is vitam D deficiency a risk factor for prostate cancer? Anticancer Res 10: 1307-1311.
6. Schwartz GG, Hill CC, Oeler TA, Becich MJ, Bahnson RR (1995) 1,25-Dihydroxy-16-ene-23-yne-vitaminD3 and prostate cancer proliferation in vivo. Urology 46: 365-369.
7. Konety BR, Schwartz GG, Acierno JS, Becich MJ, Getzenberg (1996) The role of vitamin D in normal prostate growth and differentiation. Cell Growth Diff 7: 1563-1570.
8. Lokeshwar BL (1999) Inhibition of prostate cancer metastasis in vivo: a comparison of 1,25-dihydroxy vitamin D (calcitrol) and EB1089. Cancer Epidemiol Biomark Prev 8: 241.
9. Peehl D, Feldman D (2003) The role of vitamin D and retinoids in controlling prostate cancer progression. Endocr Relat Cancer 10: 131-140.
10. Yang ES, Maiorino CA, Roos BA, Knight SR, Burnstein KL (2002) Vitamin D-mediated growth inhibition of an androgen-ablated LNCaP cell line model of human prostate cancer. Mol Cell Endocrinol 186: 69-79.
11. Goodenough DA, Paul DL (2009) Gap Junctions. Cold Spring Harbor Perspectives Biology 1: a002576.
12. Beyer EC, Berthoud VM (2009) The Family of Connexin Genes. In: Harris A, Locke D, editors. Connexins: A Guide. Springer. pp. 3-26.
13. Laird DW (2006) Life cycle of connexins in health and disease. Biochem J 394: 527-543.
14. Thevenin AF, Kowal TJ, Fong JT, Kells RM, Fisher CG, et al. (2013) Proteins and Mechanisms Regulating Gap-Junction Assembly, Internalization, and Degradation. Physiology 28: 93-116.
15. Crespin S, Defamie N, Cronier L, Mesnil M (2009) Connexins and carcinogenesis. In: Harris A, Locke D, editors. Connexinss: A Guide. pp. 529-542.
16. Naus CC, Laird DW (2010) Implications and challenges of connexin connections to cancer. Nat Rev Cancer 10: 435-441.
17. Trosko J (2006) From adult stem cells to cancer stem cells: Oct-4 Gene, cell-cell communication, and hormones during tumor promotion. Ann NY Acad Sci 1089: 36-58.
18. Trosko J (2007) Gap Junctional Intercellular Communication as a Biological "Rosetta Stone" in Understanding, in a Systems Biological Manner, Stem Cell Behavior, Mechanisms of Epigenetic Toxicology, Chemoprevention and Chemotherapy. J Memb Biol 218: 93-100.
19. Wei CJ, Xu X, Lo CW (2004) Connexins and cell signaling in development and disease. Ann Rev Cell Dev Biol 20: 811-838.
20. Xu J, Nicholson BJ (2013) The role of connexins in ear and skin physiology-Functional insights from disease-associated mutations. Biochimica et Biophysica Acta (BBA) - Biomembranes 1828: 167-178.
21. Habermann H, Chang WY, Birch L, Mehta P, Prins GS (2001) Developmental Exposure to Estrogens Alters Epithelial Cell Adhesion and Gap Junction Proteins in the Adult Rat Prostate. Endocrinology 142: 359-369.
22. Mehta PP, Perez-Stable C, Nadji M, Mian M, Asotra K, et al. (1999) Suppression of human prostate cancer cell growth by forced expression of connexin genes. Dev Genetics 24: 91-110.
23. Habermann H, Ray V, Prins G (2002) Alterations in gap junction protein expression in human benign prostatic hyperplasia and prostate cancer. J Urol 167: 655-660.
24. Govindarajan R, Song X-H, Guo R-J, Wheelock MJ, Johnson KR, et al. (2002) Impaired traffcking of connexins in androgen-independent human prostate cancer cell lines and its mitigation by a-catenin. J Biol Chem 277: 50087-50097.
25. Mitra S, Annamalai L, Chakraborty S, Johnson K, Song X, et al PP (2006) Androgen-regulated Formation and Degradation of Gap Junctions in Androgen-responsive Human Prostate Cancer Cells. Mol Biol Cell 17: 5400-5416.
26. Abate-Shen C, Shen M (2000) Molecular genetics of prostate cancer. Genes Dev 14: 2410-2434.
27. Cunha G, Donjacour A, Cooke P, Mee S, Bigsby R, et al. (1987) The endocrinology and developmental biology of the prostate. Endocr Rev 8: 338-362.
28. Marker P, Donjacour A, Dahiya R, Cunha G (2003) Hormonal, cellular, and molecular control of prostatic development. Dev Biol 253: 165-174.
29. Shen MM, Abate-Shen C (2010) Molecular genetics of prostate cancer: new prospects for old challenges. Genes & Development 24: 1967-2000.
30. Aboseif S, Dahiya R, Narayan P, Cunha G (1997) Effect of retinoic acid on prostate development. Prostate 31: 161-167.
31. Kelsey L, Katoch P, Johnson K, Batra SK, Mehta P (2012) Retinoids regulate the formation and degradation of gap junctions in androgen-responsive human prostate cancer cells. PLoS ONE 7: E32846.
32. Banach-Petrosky W, Ouyang X, Gao H, Nader K, Ji Y, et al. (2006) Vitamin D Inhibits the Formation of Prostatic Intraepithelial Neoplasia in Nkx3.1; Pten Mutant Mice. Clinical Cancer Research 12: 5895-5901.
33. Palmer HG, Gonzalez-Sancho JM, Espada J, Berciano MT, Puig I, et al. (2001) Vitamin D(3) promotes the differentiation of colon carcinoma cells by the induction of E-cadherin and the inhibition of beta-catenin signaling. J Cell Biol 154: 369-387.
34. Bertram J (1999) Carotenoids and Gene Regulation. Nutr Rev 57: 182-191.
35. King TJ, Bertram JS (2005) Connexins as targets for cancer chemoprevention and chemotherapy. Biochimica et Biophysica Acta (BBA) - Biomembranes 1719: 146-160.
36. Mehta P, Loewenstein W (1991) Differential regulation of communication by retinoic acid in homologous and heterologous junctions between normal and transformed cells. J Cell Biol 113: 371-379.
37. Mehta P, Bertram J, Loewenstein W (1989) The actions of retinoids on cellular growth correlate with their actions on gap junctional communication. J Cell Biol 108: 1053-1065.
38. Trosko J, Chang C-C (2001) Mechanism of up-regulated gap junctional intercellular communication during chemoprevention and chemotherapy of cancer. Mutat Res 480: 219-229.
39. Kojima T, Murata M, Go M, Spray DC, Sawada N (2007) Connexins induce and maintain tight junctions in epithelial cells. J Membr Biol 217: 13-19.
40. Zhao X, Ly L, Peehl D, Feldman D (1999) Induction of androgen receptor by 1alpha,25-dihydroxyvitamin D3 and 9-cis retinoic acid in LNCaP human prostate cancer cells. Endocrinology 140: 1205-1212.
41. Igawa T, Lin FF, Lee MS, Karan D, Batra SK, et al. (2002) Establishment and characterization of androgen-independent human prostate cancer LNCaP cell model. Prostate 50: 222-235.
42. Lin MF, Meng TC, Rao PS, Chang C, Schonthal AH, et al. (1998) Expression of human prostatic acid phosphatase correlates with androgen-stimulated cell proliferation in prostate cancer cell lines. J Biol Chem 273: 5939-5947.
43. Chakraborty S, Mitra S, Falk MM, Caplan S, Wheelock MJ, et al. (2010) E-cadherin differentially regulates the assembly of connexin43 and connexin32 into gap junctions in human squamous carcinoma cells. J Biol Chem 285: 10761-10776.
44. Govindarajan R, Chakraborty S, Falk MM, Johnson KR, Wheelock MJ, et al. (2010) Assembly of connexin43 is differentially regulated by E-cadherin and N-cadherin in rat liver epithelial cells. Mol Biol Cell 21: 4089-4107.
45. Johnson KE, Mitra S, Katoch P, Kelsey LS, Johnson KR, et al. (2013) Phosphorylation on Ser-279 and Ser-282 of connexin43 regulates endocytosis and gap junction assembly in pancreatic cancer cells. Mol Biol Cell 24: 715-733.
46. Glover JF, Irwin JT, Darbre PD (1988) Interaction of Phenol Red with Estrogenic and Antiestrogenic Action on Growth of Human Breast Cancer Cells ZR-75-1 and T-47-D. Cancer Research 48: 3693-3697.
47. Lin M-F, Lee MS, Garcia-Arenas R, Lin F-F (2000) Differential responsivenesss of prostatic acid phosphatae and prostate-specific antigen mRNA to androgen in prostate cancer cells. Cell Biology International 24: 681-689.
48. Mehta P, Bertram J, Loewenstein W (1986) Growth inhibition of transformed cells correlates with their junctional communication with normal cells. Cell 44: 187-196.
49. Yang ES, Burnstein KL (2003) Vitamin D Inhibits G1 to S Progression in LNCaP Prostate Cancer Cells through p27Kip1 Stabilization and Cdk2 Mislocalization to the Cytoplasm. J Biol Chem 278: 46862-46868.
50. Zhuang S-H, Burnstein KL (1998) Antiproliferative effect of 1a , 25- dihydroxyvitamin D3 in human prostate cancer cell line LNCaP involves reduction of cyclin-dependent kinease 2 activity and persistent G1 accumulation. Endocirnology 139: 1197-1207.
51. Lokeshwar B (1999) Inhibition of prostate cancer metastasis in vivo : a comparison of 1,25-dihydroxy vitamin D (calcitrol) and EB1089. Cancer Epidemiol Biomark Prev 8: 241-248.
52. Zhao X, Peehl D, Navone N, Feldman D (2000) 1alpha,25-dihydroxyvitamin D3 inhibits prostate cancer cell growth by androgen-dependent and androgen-independent mechanisms. Endocrinology 141: 2548-2556.
53. VanSlyke JK, Musil LS (2000) Analysis of connexin intracellular transport and assembly. Methods 20: 156-164.
54. Musil L, Cunningham.BA, Edelman G, Goodenough D (1990) Differential phosphorylation of the gap junction protein connexin43 in junctional communicaton-competent and -deficient cell lines. J Cell Biol 111: 2077-2088.
55. Kemppainen J, Wilson J (1996) Agonist and antigonis activities of hydroxyfluamide and casodex related to androgen receptor stabilization. Urology 48: 157-163.
56. Farla P, Hersmus R, Trapman J, Houtsmuller AB (2005) Antiandrogens prevent stable DNA-binding of the androgen receptor. Journal of Cell Science 118: 4187-4198.
57. Trosko J (2006) Dietary modulation of the multistage, multimechanisms of human carcinogenesis: effects on initiated stem cells and cell-cell communication. Nutr Cancer 94: 102-110.
58. Bosco D, Haefliger JA, Meda P (2011) Connexins: Key Mediators of Endocrine Function. Physiol Rev 91: 1393-1445.
59. Vezina C, Allgeier SMT, Fritz W, Moore R, Strerath M, et al. (2008) Retinoic acid induces prostatic bud formation. Dev Dyn 237: 1321-1333.
60. Lasnitzki I (1976) Reversal of methylchoantherene-induced changes in mouse prostates in vitro by retinoic acid and its analogues. British Journal of Cancer 34: 239-248.
61. Lasnitzki I, Goodman D (1974) Inhibition of the effects of methylcholanthrene on mouse prostate in organ culture by vitamin A and its analogs. Cancer Res 34: 1564-1571.
62. Christov KT, Moon RC, Lantvit DD, Boone CW, Steele VE, et al. (2002) 9-cisretinoic acid but not 4-(hydroxyphenyl)retinamide inhibits prostate intraepithelial neoplasia in Noble rats. Cancer Res 62: 5178-5182.
63. Manual M, Ghyselink NB, Chambon P (2006) Functions of the retinoid nuclear receptors: Lessons from the genetic and pharmacological dissections of the retinoic acid signaling pathway during mouse embyrogenesis. Ann Rev Pharm Tox 46: 451-480.
64. Swami S, Krishnan AV, Wang JY, Jensen K, Horst R, et al. (2012) Dietary Vitamin D3 and 1,25-Dihydroxyvitamin D3 (Calcitriol) Exhibit Equivalent Anticancer Activity in Mouse Xenograft Models of Breast and Prostate Cancer. Endocrinology 153: 2576-2587.
65. VanSlyke JK, Deschenes SM, Musil LS (2001) Intracellular transport, assembly, and degradation of wild-type and disease-linked mutant gap junction proteins. Mol Biol Cell 11: 1933-1946.
66. Iversen P (2002) Antiandrogen monotherapy: indications and results. Urology 60: 64-71.
67. Kokai Y, Murata M, Go M, Spray DC, Sawada N (2011) Connexins induce and maintain tight junctions in epithelial cells. J Membr Biol 217: 13-19.
68. Kojima T, Kokai Y, Chiba H, Yamamoto M, Mochizuki Y, et al. (2001) Cx32 but Not Cx26 Is Associated with Tight Junctions in Primary Cultures of Rat Hepatocytes. Experimental Cell Research 263: 193-201.
69. Kojima T, Spray DC, Kokai Y, Chiba H, Mochizuki Y, et al. (2002) Cx32 formation and/or Cx32-mediated intercellular communication induces expression and function of tight junctions in hepatocytic cell line. Exp Cell Res 276: 40-51.
70. Shen R, Sumitomo M, Dai J, Harris A, Kaminetzky D, et al. (2000) Androgen-Induced Growth Inhibition of Androgen Receptor Expressing Androgen-Independent Prostate Cancer Cells Is Mediated by Increased Levels of Neutral Endopeptidase. Endocrinology 141: 1699.
71. Zhuang S-H, Schwartz GG, Cameron D, Burnstein KL (1997) Vitamin D receptor content and transcriptional activity do not fully predict antiproliferative effects of vitamin D in human prostate cancer cell lines. Mol Cell Endo 83-90.
72. Wang M, Berthoud VM, Beyer EC (2007) Connexin43 increases the sensitivity of prostate cancer cells to TNF{alpha}-induced apoptosis. Journal of Cell Science 120: 320-329.
73. Hirschi KK, Xu C, Tsukamoto T, Sager R (1996) Gap junction genes Cx26 and Cx43 individually suppress the cancer phenotype of human mammary carcinoma cells and restore differentiation potential. Cell Growth Diff 7: 861-870.
74. Mao AJ, Bechberger J, Lidington D, Galipeau J, Laird DW, et al. (2000) Neuronal Differentiation and Growth Control of Neuro-2a Cells After Retroviral Gene Delivery of Connexin43. The Journal of Biological Chemistry 275: 34407-34414.
75. Langlois SP, Cowan KN, Shao Q, Cowan BJ, Laird DW (2010) The Tumor- Suppressive Function of Connexin43 in Keratinocytes Is Mediated in Part via Interaction with Caveolin-1. Cancer Research 70: 4222-4232.
76. Langlois S, Maher AC, Manias JL, Shao Q, Kidder GM, et al. (2007) Connexin Levels Regulate Keratinocyte Differentiation in the Epidermis. J Biol Chem 282: 30171-30180.
77. McLachlan E, Shao Q, Wang Hl, Langlois S, Laird DW (2006) Connexisn act as tumor suppressors in three dimensional mammary cell organoids by regulating differentiation and angiogenesis. Cancer Res 66: 9886-9894.
78. Plante I, Stewart MKG, Barr K, Allan AL, Laird DW (2010) Cx43 suppresses mammary tumor metastasis to the lung in a Cx43 mutant mouse model of human disease. Oncogene 30: 1681-1692.
79. Kardami E, Dang X, Iacobas DA, Nickel BE, Jeyaraman M, et al. (2007) The role of connexins in controlling cell growth and gene expression. Progress in Biophysics and Molecular Biology 94: 245-264.
80. King TJ, Lampe PD (2005) Altered tumor biology and tumorigenesis in irradiated and chemical carcinogen-treated single and combined connexin32/ p27Kip1-deficient mice. Communication and Cell Adhesion 293-305.
81. King TJ, Lampe PD (2004) Mice deficient for the gap junction protein Connexin32 exhibit increased radiation-induced tumorigenesis associated with elevated mitogen-activated protein kinase (p44/Erk1, p42/Erk2) activation. Carcinogenesis 25: 669-680.
82. King TJ, Gurley KE, Prunty J, Shin JL, Kemp CJ, et al. (2005) Deficiency in the gap junction protein connexin32 alters p27Kip1 tumor suppression and MAPK activation in a tissue-specific manner. Oncogene 24: 1718-1726.
83. 1. Endocirnology 138: 1491-1497.
84. 3receptors and actions in human prostate cancer cell lines. Endocrinology 132: 1952-1960.
85. Chen S-C, Pelletier DB, Ao P, Boynton AL (1995) Connexin43 reverses the phenotype of transformed cells and alters their expression of cyclin/cyclin-dependent kinases. Cell Growth Diff 6: 681-690.
86. Laird DW (2010) The gap junction proteome and its relationship to disease. Trends Cell Biol 20: 92-101.
87. Paluch E, Heisenberg CP (2009) Biology and Physics of Cell Shape Changes in Development. Current Biology 19: R790-R799.
88. Salbreux G, Charras G, Paluch E (2012) Actin cortex mechanics and cellular morphogenesis. Trends In Cell Biology 22: 536-545.
89. Francis R, Xu X, Park H-D, Wei J-C, Chang S, et al. (2012) Connexin43 modulates cell polarity and directional cell migration by regulating microtubule dynamics. PLoS ONE 6: 1-14.
90. Schwartz G, Hulka BS (1990) Is vitamin D deficiency a risk factor for prostate cancer? Anticancer Res 10: 1307-1311.
91. Ahn J, Peters U, Albanes D, Purdue MP, Abnet CC, et al. (2008) Serum Vitamin D Concentration and Prostate Cancer Risk: A Nested CaseΓÇôControl Study. Journal of the National Cancer Institute 100: 796-804.
92. Bostwick DG, Qian J (2004) High-grade prostatic intraepithelial neoplasia. Mod Pathol 17: 360-379.
93. Bostwick DG (1992) Prostatic intraepithelial neoplasia (PIN): current concepts. J Cell Biochem 16H: 10-19.