Unexpected induction of the human connexin 43 promoter by the Ras signaling pathway is mediated by a novel putative promoter sequence

Molecular Pharmacology

Volumn 63, Issue 4, 2003, Pages 821-831

  Carystinos, George D ^a   Kandouz, Mustapha ^a   Alaoui Jamali, Moulay A ^a   Batist, Gerald ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; CONNEXIN 43; GELDANAMYCIN; HEAT SHOCK PROTEIN 90; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; PROTEIN KINASE P60;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; CELL STRAIN 3T3; CELL STRAIN MCF 7; CONTROLLED STUDY; DNA BINDING; GEL MOBILITY SHIFT ASSAY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCOGENE C MYC; ONCOGENE H RAS; PRIORITY JOURNAL; PROMOTER REGION; PROTO ONCOGENE; RAT; SIGNAL TRANSDUCTION; SURVIVAL;

3T3 CELLS; ANIMALS; CONNEXIN 43; FEMALE; GENE EXPRESSION; GENES, RAS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; MICE; PROMOTER REGIONS (GENETICS); PROTO-ONCOGENE PROTEINS C-MYC; SIGNAL TRANSDUCTION;

EID: 0037382251     PISSN: 0026895X     EISSN: None     Source Type: Journal    
DOI: 10.1124/mol.63.4.821     Document Type: Article

References (85)

1. Albright CD, Jones RT, Grimley PM, and Resau JH (1990) Intercellular communication in bronchial epithelial cells: review of evidence for a possible role in lung carcinogenesis. Toxicol Pathol 18:324-341.
2. Bao X, Clark CB, and Frangos JA (2000) Temporal gradient in shear-induced signaling pathway: involvement of MAP kinase, c-fos and connexin43. Am J Physiol Heart Circ Physiol 278:H1598-H1605.
3. Behre G, Smith LT, and Tenen DG (1999) Use of a promoterless Renilla luciferase vector as an internal control plasmid for transient co-transfection assays of Ras-mediated transcription activation. Biotechniques 26:24-6:28.
4. Brissette JL, Kumar NM, Gilula NB, and Dotto GP (1991) The tumor promoter 12-O-tetradecanoylphorbol-13-acetate and the ras oncogene modulate expression and phosphorylation of gap junction proteins. Molh Cell Biol 11:5364-5371.
5. Bruzzone R, White TW, and Paul DL (1996) Connections with connexins: the molecular basis of direct intercellular signaling. Eur J Biochem 238:1-27.
6. Burgering BM and Bos JL (1995) Regulation of Ras-mediated signalling: more than one way to skin a cat. Trends Biochem Sci 20:18-22.
7. Campbell SL, Khosravi-Far R, Rossman KL, Clark GJ, and Der CJ (1998) Increasing complexity of Ras signaling. Oncogene 17:1395-1413.
8. Caruso JA, Laird DW, and Batist G (1999) Role of HSP90 in mediating cross-talk between the estrogen receptor and the Ah receptor signal transduction pathways. Biochem Pharmacol 58:1395-1403.
9. Carystinos GD, Katabi MM, Laird DW, Galipeau J, Chan H, Alaoui-Jamali MA, and Batist G (1999) Cyclic-AMP induction of gap junctional intercellular communication increases bystander effect in suicide gene therapy. Clin Cancer Res 5:61-68.
10. Charles AC, Naus CC, Zhu D, Kidder GM, Dirksen ER, and Sanderson MJ (1992) Intercellular calcium signaling via gap junctions in glioma cells. J Cell Biol 118:195-201.
11. Cowan DB, Lye SJ, and Langille BL (1998) Regulation of vascular connexin43 gene expression by mechanical loads. Circ Res 82:786-793.
12. DeFranco DB, Ramakrishnan C, and Tang Y (1998) Molecular chaperones and subcellular trafficking of steroid receptors. J Steroid Biochem Mol Biol 65:51-58.
13. Echetebu CO, Ali M, Izban MG, MacKay L, and Garfield RE (1999) Localization of regulatory protein binding sites in the proximal region of human myometrial connexin 43 gene. Mol Hum Reprod 5:757-766.
14. Fernandez-Cobo M, Stewart D, Drujan D, De Maio (2001) A. Promoter activity of the rat connexin 43 gene in NRK cells. J Cell Biochem 81:514-522.
15. Freeman SM, Abboud CN, Whartenby KA, Packman CH, Koeplin DS, Moolten FL, and Abraham GN (1993) The "bystander effect": tumor regression when a fraction of the tumor mass is genetically modified. Cancer Res 53:5274-5283.
16. Geimonen E, Jiang W, Ali M, Fishman GI, Garfield RE, and Andersen J (1996) Activation of protein kinase C in human uterine smooth muscle induces connexin-43 gene transcription through an AP-1 site in the promoter sequence. J Biol Chem 271:23667-23674.
17. Gire V, Marshall C, and Wynford-Thomas D (2000) PI-3-kinase is an essential anti-apoptotic effector in the proliferative response of primary human epithelial cells to mutant RAS. Oncogene 19:2269-2276.
18. Goodenough DA, Goliger JA, and Paul DL (1996) Connexins, connexons and intercellular communication. Annu Rev Biochem 65:475-502.
19. Grammatikakis N, Lin JH, Grammatikakis A, Tsichlis PN, and Cochran BH (1999) p50(cdc37) acting in concert with Hsp90 is required for Raf-1 function. Mol Cell Biol 19:1661-1672.
20. Grenert JP, Sullivan WP, Fadden P, Haystead TAJ, Clark J, Mimnaugh E, Krutzsch H, Ochel HJ, Schulte TW, Sausville E, Neckers LM, and Toft DO (1997) The amino-terminal domain of heat shock protein 90 (hsp90) that binds geldanamycin is an ATP/ADP switch domain that regulates hsp90 conformation. J Biol Chem 272:23843-23850.
21. Hofer A, Saez JC, Chang CC, Trosko JE, Spray DC, and Dermietzel R (1996) C-erbB2/neu transfection induces gap junctional communication incompetence in glial cells. J Neurosci 16:4311-4321.
22. Holden PR, McGuire B, Stoler A, Balmain A, and Pitts JD (1997) Changes in gap junctional intercellular communication in mouse skin carcinogenesis. Carcinogenesis 18:15-21.
23. Hossain MZ, Ao P, and Boynton AL (1998) Platelet-derived growth factor-induced disruption of gap junctional communication and phosphorylation of connexin43 involves protein kinase C and mitogen-activated protein kinase. J Cell Physiol 176:332-341.
24. Hossain MZ, Jagdale AB, Ao P and Boynton AL (1999a) Mitogen-activated protein kinase and phosphorylation of connexin43 are not sufficient for the disruption of gap junctional communication by platelet-derived growth factor and tetradecanoylphorbol acetate. J Cell Physiol 179:87-96.
25. Hossain MZ, Jagdale AB, Ao P, Kazlauskas A, and Boynton AL (1999b) Disruption of gap junctional communication by the platelet-derived growth factor is mediated via multiple signaling pathways. J Biol Chem 274:10489-10496.
26. Huang RP, Hossain MZ, Sehgal A, and Boynton AL (1999) Reduced connexin43 expression in high-grade human brain glioma cells. J Surg Oncol 70:21-24.
27. Huang W, Alessandrini A, Crews CM, and Erikson RL (1993) Raf-1 forms a stable complex with Mek1 and activates Mek1 by serine phosphorylation. Proc Natl Acad Sci USA 90:10947-10951.
28. Janssen RA, Veenstra KG, Jonasch P, Jonasch E, and Mier JW (1998) Ras- and Raf-induced down-modulation of non-muscle tropomyosin are MEK-independent. J Biol Chem 273:32182-32186.
29. Jou YS, Layhe B, Matesic DF, Chang CC, de Feijter AW, Lockwood L, Welsch CW, Klaunig JE, and Trosko JE (1995) Inhibition of gap junctional intercellular communication and malignant transformation of rat liver epithelial cells by neu oncogene. Carcinogenesis 16:311-317.
30. Kam Y, Kim DY, Koo SK, and Joe CO (1998) Transfer of second messengers through gap junction connexin 43 channels reconstituted in liposomes. Biochim Biophys Acta 1372:384-388.
31. Kerkhoff E, Houben R, Loffler S, Troppmair J, Lee JE, and Rapp UR (1998) Regulation of c-myc expression by Ras/Raf signalling. Oncogene 16:211-216.
32. Kauffmann-Zeh A, Rodriguez-Viciana P, Ulrich E, Gilbert C, Coffer P, Downward J, and Evan G (1997) Suppression of c-Myc-induced apoptosis by Ras signalling through PI(3)K and PKB. Nature (Lond) 385:544-548.
33. Kerkhoff E and Rapp UR (1998) High-intensity Raf signals convert mitotic cell cycling into cellular growth. Cancer Res 58:1636-1640.
34. Kerkhoff E, Houben R, Loffler S, Troppmair J, Lee JE, and Rapp UR (1998) Regulation of c-myc expression by Ras/Raf signalling. Oncogene 16:211-216.
35. Knutson A, Castano E, Oelgeschlager T, Roeder RG, and Westin G (2000) Down-stream promoter sequences facilitate the formation of a specific transcription factor IID-promoter complex topology required for efficient transcription from the megalin/low density lipoprotein receptor-related protein 2 promoter. J Biol Chem 275:14190-14197.
36. Kutach AK and Kadonaga JT (2000) The downstream promoter element DPE appears to be as widely used as the TATA box in Drosophila core promoters. Mol Cell Biol 20:4754-4764.
37. Laird DW, Castillo M, and Kasprzak L (1995) Gap junction turnover, intracellular trafficking and phosphorylation of connexin43 in brefeldin A-treated rat mammary tumor cells. J Cell Biol 131:1193-1203.
38. Laird DW, Fistouris P, Batist G, Alpert L, Huynh HT, Carystinos GD, and Alaoui-Jamali MA (1999) Deficiency of connexin43 gap junctions is an independent marker for breast tumors. Cancer Res 59:4104-4110.
39. Lee SW, Tomasetto C, Paul D, Keyomarsi K, and Sager R (1992) Transcriptional downregulation of gap-junction proteins blocks junctional communication in human mammary tumor cell lines. J Cell Biol 118:1213-1221.
40. Lemaitre JM, Bocquet S, Buckle R, and Mechali M (1995) Selective and rapid nuclear translocation of a c-Myc-containing complex after fertilization of Xenopus laevis eggs. Mol Cell Biol 15:5054-5062.
41. Lin AW, Barradas M, Stone JC, van Aelst L, Serrano M, and Lowe SW (1998) Premature senescence involving p53 and p16 is activated in response to constitutive MEK/MAPK mitogenic signaling. Genes Dev 12:3008-3019.
42. Loo LW, Kanemitsu MY, and Lau AF (1999) In vivo association of pp60v-src and the gap-junction protein connexin 43 in v-src-transformed fibroblasts. Mol Carcinog 25:187-195.
43. Lundberg AS, Randell SH, Stewart SA, Elenbaas B, Hartwell KA, Brooks MW, Fleming MD, Olsen JC, Miller SW, Weinberg RA, and Hahn WC (2002) Immortalization and transformation of primary human airway epithelial cells by gene transfer. Oncogene 21:4577-4586).
44. Marshall CJ (1996) Ras effectors. Curr Opin Cell Biol 8:197-204.
45. Mehta PP, Hotz-Wagenblatt A, Rose B, Shalloway D, and Loewenstein WR (1991) Incorporation of the gene for a cell-cell channel protein into transformed cells leads to normalization of growth. J Membr Biol 124:207-225.
46. Mesnil M, Piccoli C, Tiraby G, Willecke K, and Yamasaki H (1996) Bystander killing of cancer cells by herpes simplex virus thymidine kinase gene is mediated by connexins. Proc Natl Acad Sci USA 93:1831-1835.
47. Miele C, Rochford JJ, Filippa N, Giorgetti-Peraldi S, and Van Obberghen E (2000) Insulin and insulin-like growth factor-I induce vascular endothelial growth factor mRNA expression via different signaling pathways [In Process Citation]. J Biol Chem 275:21695-21702.
48. Mitchell JA, Ou C, Chen Z, Nishimura T, and Lye SJ (2001) Parathyroid hormone-induced up-regulation of connexin-43 mRNA is mediated by sequences within both the promoter and the 3′ untranslated region of the mRNA. Endocrinology 142:907-915.
49. Nagy JI, Hossain MZ, Lynn BD, Curpen GE, Yang S, and Turley EA (1996) Increased connexin-43 and gap junctional communication correlate with altered phenotypic characteristics of cells overexpressing the receptor for hyaluronic acid-mediated motility. Cell Growth & Differentiation 7:745-751.
50. Nicolson GL, Dulski KM, and Trosko JE (1988) Loss of intercellular junctional communication correlates with metastatic potential in mammary adenocarcinoma cells. Proc Natl Acad Sci USA 85:473-476.
51. Osborn L, Kunkel S, and Nabel GJ (1989) Tumor necrosis factor alpha and interleukin 1 stimulate the human immunodeficiency virus enhancer by activation of the nuclear factor kappa B. Proc Natl Acad Sci USA 86:2336-2340.
52. Postma FR, Hengeveld T, Alblas J, Giepmans BN, Zondag GC, Jalink K, and Moolenaar WH (1998) Acute loss of cell-cell communication caused by G protein-coupled receptors: a critical role for c-Src. J Cell Biol 140:1199-1209.
53. Pratt WB (1993) The role of heat shock proteins in regulating the function, folding and trafficking of the glucocorticoid receptor. J Biol Chem 268:21455-21458.
54. Pratt WB, Silverstein AM, and Galigniana MD (1999) A model for the cytoplasmic trafficking of signalling proteins involving the hsp90-binding immunophilins and p50cdc37. Cell Signal 11:839-851.
55. Proulx AA, Lin ZX, and Naus CC (1997) Transfection of rhabdomyosarcoma cells with connexin43 induces myogenic differentiation. Cell Growth Differ 8:533-540.
56. Rose B, Mehta PP, and Loewenstein WR (1993) Gap-junction protein gene suppresses tumorigenicity. Carcinogenesis 14:1073-1075.
57. Roy S, Wyse B, and Hancock JF (2002) H-ras signaling and k-ras signaling are differentially dependent on endocytosis. Mol Cell Biol 22:5128-5140.
58. Sakamuro D and Prendergast GC (1999) New Myc-interacting proteins: a second Myc network emerges. Oncogene 18:2942-2954.
59. Saphire AC, Bark SJ, and Gerace L (1998) All four homochiral enantiomers of a nuclear localization sequence derived from c-Myc serve as functional import signals. J Biol Chem 273:29764-29769.
60. Schiavi A, Hudder A, and Werner R (1999) Connexin43 mRNA contains a functional internal ribosome entry site. FEBS Lett 464:118-122.
61. Schulte TW, An WG, and Neckers LM (1997) Geldanamycin-induced destabilization of Raf-1 involves the proteasome. Biochem Biophys Res Commun 239:655-659.
62. Sears R, Leone G, DeGregori J, and Nevins JR (1999) Ras enhances Myc protein stability. Mol Cell 3:169-179.
63. Silverstein AM, Grammatikakis N, Cochran BH, Chinkers M, and Pratt WB (1998) p50(cdc37) binds directly to the catalytic domain of Raf as well as to a site on hsp90 that is topologically adjacent to the tetratricopeptide repeat binding site. J Biol Chem 273:20090-20095.
64. Stancato LF, Silverstein AM, Owens-Grillo JK, Chow YH, Jove R, and Pratt WB (1997) The hsp90-binding antibiotic geldanamycin decreases Raf levels and epidermal growth factor signaling without disrupting formation of signaling complexes or reducing the specific enzymatic activity of Raf kinase. J Biol Chem 272:4013-4020.
65. Stock A and Sies H (2000) Thyroid hormone receptors bind to an element in the connexin43 promoter. Biol Chem 381:973-979.
66. Tabin CJ, Bradley SM, Bargmann CI, Weinberg RA, Papageorge AG, Scolnick EM, Dhar R, Lowy DR, and Chang EH (1982) Mechanism of activation of a human oncogene. Nature (Lond) 300:143-149.
67. Tomakidi P, Cheng H, Kohl A, Komposch G, and Alonso A (2000) Connexin 43 expression is downregulated in raft cultures of human keratinocytes expressing the human papillomavirus type 16E5 protein. Cell Tissue Res 301(2):323-327.
68. Toyofuku T, Yabuki M, Otsu K, Kuzuya T, Tada M, and Hori M (1999) Functional role of c-Src in gap junctions of the cardiomyopathic heart [see comments]. Circ Res 85:672-681.
69. Trosko JE and Goodman JI (1994) Intercellular communication may facilitate apoptosis: implications for tumor promotion, Mol Carcinog 11:8-12.
70. Trosko JE and Ruch RJ (1998) Cell-cell communication in carcinogenesis [In Process Citation]. Front Biosci 3:D208-D236.
71. Tsai H, Werber J, Davia MO, Edelman M, Tanaka KE, Melman A, Christ GJ, and Geliebter J (1996) Reduced connexin 43 expression in high grade, human prostatic adenocarcinoma cells. Biochem Biophys Res Commun 227:64-69.
72. Umhauer S, Ruch RJ, and Fanning J (2000) Gap junctional intercellular communication and connexin 43 expression in ovarian carcinoma. Am J Obstet Gynecol 182:999-1000.
73. van Aelst L, Barr M, Marcus S, Polverino A, and Wigler M (1993) Complex formation between RAS and RAF and other protein kinases. Proc Natl Acad Sci USA 90:6213-6217.
74. van der Heyden MA, Rook MB, Hermans MM, Rijksen G, Boonstra J, Defize LH, and Destree OH (1998) Identification of connexin43 as a functional target for Wnt signalling. J Cell Sci 111, 1741-1749.
75. Vasilevskaya IA and O'Dwyer PJ (1999) Effects of geldanamycin on signaling through activator-protein 1 in hypoxic HT29 human colon adenocarcinoma cells. Cancer Res 59:3935-3940.
76. Veenstra GJC and Wolffe AP (2001) Gene-selective developmental roles of general transcription factors. Trends in Biochem Sci 26:665-671.
77. Vojtek AB and Der CJ (1998) Increasing complexity of the Ras signaling pathway. J Biol Chem 273:19925-19928.
78. Warn-Cramer BJ, Cottrell GT, Burt JM, and Lau AF (1998) Regulation of connexin-43 gap junctional intercellular communication by mitogen-activated protein kinase. J Biol Chem 273:9188-9196.
79. Warn-Cramer BJ, Lampe PD, Kurata WE, Kanemitsu MY, Loo LW, Eckhart W, and Lau AF (1996) Characterization of the mitogen-activated protein kinase phosphorylation sites on the connexin-43 gapjunction protein. J Biol Chem 271:3779-3786.
80. Yamasaki H (1990) Gap junctional intercellular communication and carcinogenesis. Carcinogenesis 11:1051-1058.
81. Yamasaki H, Mesnil M, Omori Y, Mironov N, and Krutovskikh V (1995) Intercellular communication and carcinogenesis. Mutat Res 333:181-188.
82. Zhou L, Kasperek EM, and Nicholson BJ (1999) Dissection of the molecular basis of pp60(v-src) induced gating of connexin 43 gap junction channels. J Cell Biol 144:1033-1045.
83. Zhu D, Kidder GM, Caveney S, and Naus CC (1992) Growth retardation in glioma cells cocultured with cells overexpressing a gap junction protein. Proc Natl Acad Sci USA 89:10218-10221.
84. Zhu D, Caveney S, Kidder GM, and Naus CC (1991) Transfection of C6 glioma cells with connexin 43 cDNA: analysis of expression, intercellular coupling and cell proliferation. Proc Natl Acad Sci USA 88:1883-1887.
85. Zhu J, Woods D, McMahon M, and Bishop JM (1998) Senescence of human fibroblasts induced by oncogenic Raf. Genes Dev 12:2997-3007.