Nicotine promotes apoptosis resistance of breast cancer cells and enrichment of side population cells with cancer stem cell-like properties via a signaling cascade involving galectin-3, α9 nicotinic acetylcholine receptor and STAT3

Breast Cancer Research and Treatment

Volumn 145, Issue 1, 2014, Pages 5-22

  Guha, Prasun ^a,b   Bandyopadhyaya, Gargi ^a,b   Polumuri, Swamy K ^a   Chumsri, Saranya ^a,c   Gade, Padmaja ^a   Kalvakolanu, Dhananjaya V ^a,c   Ahmed, Hafiz ^a,b,c  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MARYLAND CENTER FOR ENVIRONMENTAL SCIENCE   (United States)

^c UNIVERSITY OF MARYLAND   (United States)

Author keywords

Apoptosis; Galectin 3; Metastatic cancer; Nicotine; Stem cell

Indexed keywords

ALPHA9 NICOTINIC ACETYLCHOLINE RECEPTOR; CELL PROTEIN; GALECTIN 3; NICOTINE; NICOTINIC RECEPTOR; PROTEIN TWIST1; STAT3 PROTEIN; UNCLASSIFIED DRUG; CHRNA9 PROTEIN, HUMAN; NICOTINIC AGENT; STAT3 PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL LINE; CANCER RESISTANCE; CANCER STEM CELL; CONTROLLED STUDY; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIMARY TUMOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SEQUENCE ANALYSIS; SIDE POPULATION CELL; SIGNAL TRANSDUCTION; UNINDEXED SEQUENCE; UPREGULATION; BIOSYNTHESIS; BREAST TUMOR; CHROMATIN IMMUNOPRECIPITATION; DNA FRAGMENTATION; DRUG EFFECTS; GENETIC TRANSFECTION; IMMUNOHISTOCHEMISTRY; METABOLISM; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; TUMOR CELL LINE; WESTERN BLOTTING;

APOPTOSIS; BLOTTING, WESTERN; BREAST NEOPLASMS; CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; DNA FRAGMENTATION; GALECTIN 3; HUMANS; IMMUNOHISTOCHEMISTRY; NEOPLASTIC STEM CELLS; NICOTINE; NICOTINIC AGONISTS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, NICOTINIC; SIDE-POPULATION CELLS; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TRANSFECTION;

EID: 84900468131     PISSN: 01676806     EISSN: 15737217     Source Type: Journal    
DOI: 10.1007/s10549-014-2912-z     Document Type: Article

References (61)

1. Adhikari B, Kahende J, Malarcher A, Pechacek T, Tong V (2008) Smoking-attributable mortality, years of potential life lost, and productivity losses - United States, 2000-2004. Morbidity and Mortality Weekly Rep 2008, 57:1226-1228
2. Singh S, Pillai S, Chellappan S (2011) Nicotinic acetylcholine receptor signaling in tumor growth and metastasis. J Oncol 2011:456743
3. Nishioka T, Kim HS, Luo LY, Huang Y, Guo J, Chen CY (2011) Sensitization of epithelial growth factor receptors by nicotine exposure to promote breast cancer cell growth. Breast Cancer Res 13:R113
4. Momi N, Ponnusamy MP, Kaur S, Rachagani S, Kunigal SS, Chellappan S, Ouellette MM, Batra SK (2013) Nicotine/cigarette smoke promotes metastasis of pancreatic cancer through α9 nAChR-mediated MUC4 upregulation. Oncogene 32:1384-1395
5. Dasgupta P, Kinkade R, Joshi B, Decook C, Haura E, Chellappan S (2006) Nicotine inhibits apoptosis induced by chemotherapeutic drugs by up-regulating XIAP and surviving. Proc Natl Acad Sci USA 103:6332-6337
6. Shih YL, Liu HC, Chen CS, Hsu CH, Pan MH, Chang HW, Chen FC, Ho CT, Yang YY, Ho YS (2010) Combination treatment with luteolin and quercetin enhances antiproliferative effects in nicotine-treated MDA-MB-231 cells by down regulating nicotinic acetylcholine receptors. J Agric Food Chem 58:235-241
7. Levy DE, Darnell JE Jr (2002) Stats: transcriptional control and biological impact. Nat Rev Mol Cell Biol 3:651-662
8. Takemoto S, Ushijima K, Kawano K, Yamaguchi T, Terada A, Fujiyoshi N, Nishio S, Tsuda N, Ijichi M, Kakuma T et al (2009) Expression of activated signal transducer and activator of transcription-3 predicts poor prognosis in cervical squamous-cell carcinoma. Br J Cancer 101:967-972
9. Ryu K, Choy E, Yang C, Susa M, Hornicek FJ, Mankin H, Duan Z (2010) Activation of signal transducer and activator of transcription 3 (Stat3) pathway in osteosarcoma cells and overexpression of phosphorylated-Stat3 correlates with poor prognosis. J Orthop Res 28:971-980
10. Chen RJ, Ho YS, Guo HR, Wang YJ (2010) Long-term nicotine exposure-induced chemoresistance is mediated by activation of Stat3 and downregulation of ERK1/2 via nAChR and beta-adrenoreceptors in human bladder cancer cells. Toxicol Sci 115:118-130
11. Macha MA, Matta A, Chauhan SS, Siu KW, Ralhan R (2011) Guggulsterone (GS) inhibits ST/Nicotine modulated NF-kB and STAT3 pathways in oral cancer SCC4 cells. Carcinogenesis 32:368-380
12. Xu TY, Guo LL, Wang P, Song J, Le YY, Viollet B, Miao CY (2012) Chronic exposure of nicotine enhances insulin sensitivity though α7 nicotinic acetylcholine receptor-STAT3 pathway. PLoS ONE 7:e51217
13. Liu FT, Rabinovich GA (2005) Galectins as modulators of tumor progression. Nat Rev Cancer 5:29-41
14. Radosavljevic G, Volarevic V, Jovanovic I, Milovanovic M, Pejnovic N, Arsenijevic N, Hsu DK, Lukic ML (2012) The roles of galectin-3 in autoimmunity and tumor progression. Immunol Res 52:100-110
15. Rabinovich GA, van Kooyk Y, Cobb BA (2012) Glycobiology of immune responses. Ann NY Acad Sci 1253:1-15
16. Guha P, Kaptan E, Bandypadhyaya G, Kaczanowska S, Davila E, Thompson K, Martin SS, Kalvakolanu DK, Vasta GR, Ahmed H (2013) Cod glycopeptides with picomolar affinity to galectin-3 suppresses T-cell apoptosis and prostate cancer metastasis. Proc Natl Acad Sci USA 110:5052-5057
17. Hsu DK, Dowling CA, Jeng KC, Chen JT, Yang RY, Liu FT (1999) Galectin-3 expression is induced cirrhotic liver and hepatocellular carcinoma. Int J Cancer 81:519-526
18. Miyazaki J, Hokari R, Kato S, Tsuzuki Y, Kawaguchi A, Nagao S, Itoh K, Miura S (2002) Increased expression of Galectin-3 in primary gastric cancer and the metastatic lymph nodes. Oncol Rep 9:1307-1312
19. Yoshimura A, Gemma A, Hosoya Y, Komaki E, Hosomi Y, Okano T, Takenaka K, Matuda K, Seike M, Uematsu K et al (2003) Increased expression the LGALS3 (galectin 3) gene in human non-small-cell lung cancer. Genes Chromosomes Cancer 37:159-164
20. Saussez S, Decaestecker C, Mahillon V, Cludts S, Capouillez A, Chevalier D, Vet HK, André S, Toubeau G, Leroy X et al (2008) Galectin-3 up-regulation during tumor progression in head and neck cancer. Laryngoscope 118:1583-1590
21. Lotz MM, Andrews CW Jr, Korzeliu CA, Lee EC, Steele GD Jr, Clarke A, Mercurio AM (1993) Decreased expression of Mac-2 (carbohydrate binding protein 35) and loss of its localization are associated with the neoplastic progression of colon carcinoma. Proc Natl Acad Sci USA 90:3466-3470
22. Honjo Y, Inohara H, Akahani S, Yoshii T, Takenaka Y, Yoshida J, Hattori K, Tomiyama Y, Raz A, Kubo T (2000) Expression of cytoplasmic galectin-3 as a prognostic marker in tongue carcinoma. Clin Cancer Res 6:4635-4640
23. Nakahara S, Oka N, Raz A (2005) On the role of galectin-3 in cancer apoptosis. Apoptosis 10:267-275
24. Wang Y, Nangia-Makker P, Tait L, Balan V, Hogan V, Pienta KJ, Raz A (2009) Regulation of prostate cancer progression by galectin-3. Am J Pathol 174:1515-1523
25. Burlacu A (2003) Regulation of apoptosis by by Bcl-2 family proteins. J Cell Mol Med 7:249-257
26. Glinsky GV, Price JE, Glinsky VV, Mossine VV, Kiriakova G, Metcalf JB (1996) Inhibition of human breast cancer metastasis in nude mice by synthetic glycoamines. Cancer Res 56:5319-5324
27. Johnson KD, Glinskii OV, Mossine VV, Turk JR, Mawhinney TP, Anthony DC, Henry CJ, Huxley VH, Glinsky GV, Pienta KJ, Raz A, Glinsky VV (2007) Galectin-3 as a potential therapeutic target in tumors arising from malignant endothelia. Neoplasia 9:662-670
28. Glinsky VV, Kiriakova G, Glinskii OV, Mossine VV, Mawhinney TP, Turk JR, Glinskii AB, Huxley VH, Price JE, Glinsky GV (2009) Synthetic galectin-3 inhibitor increases metastatic cancer cell sensitivity to taxol-induced apoptosis in vitro and in vivo. Neoplasia 11:901-909
29. Glinskii OV, Sud S, Mossine VV, Mawhinney TP, Anthony DC, Glinsky GV, Pienta KJ, Glinsky VV (2012) Inhibition of Prostate Cancer Bone Metastasis by Synthetic TF Antigen Mimic/Galectin-3 Inhibitor Lactulose-l-Leucine. Neoplasia 14:65-73
30. Sun P, Nallar SC, Kalakonda S, Lindner DJ, Martin SS, Kalvakolanu DV (2009) GRIM-19 inhibits v-Src-induced cell motility by interfering with cytoskeletal restructuring. Oncogene 28:1339-1347
31. Ahmed H, Cappello F, Rodolico V, Vasta GR (2009) Evidence of heavy methylation in the galectin-3 promoter in early stages of prostate- adenocarcinoma: development and validation of a methylated marker for early diagnosis of prostate cancer. Transl Oncol 2:146-156
32. Banerjee A, Lang JY, Hung MC, Sengupta K, Banerjee SK, Baksi K, Banerjee DK (2011) Unfolded protein response is required in nu/nu mice microvasculature for treating breast tumor with tunicamycin. J Biol Chem 286:29127-29138
33. Sierra J, Villagra A, Paredes R, Cruzat F, Gutierrez S, Javed A, Arriagada G, Olate J, Imschenetzky M, Van Wijnen AJ et al (2003) Regulation of bone-specific osteocalcin gene by p300 requires Runx2/Cbfa1and the vitamin D3 receptor but not p300 intrinsic histone acetyltransferase activity. Mol Cell Biol 23:3339-3351
34. Guo J, Ibaragi S, Zhu T, Luo LY, Hu GF, Huppi PS, Chen CY (2008) Nicotine promotes mammary tumor migration via a signaling cascade involving PKC and ccd42. Cancer Res 68:8473-8481
35. Kondo T, Setoguchi T, Taga T (2004) Persistence of a small subpopulation of cancer-stem like cells in the C6 glioma cell line. Proc Natl Acad Sci USA 101:781-786
36. Telford WG, Bradford J, Godfrey W, Robey RW, Bates SE (2007) Side population analysis using a violet-excited cell-permeable DNA binding dye. Stem Cells 25:1029-1036
37. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ, Wicha MS (2003) In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 17:1253-1270
38. Dasgupta P, Rizwani W, Pillai S, Kinkade R, Kovacs M, Rastogi S, Banerjee S, Carless M, Kim E, Coppola D et al (2009) Nicotine induces cell proliferation, invasion and epithelial-mesenchymal transition in a variety of human cancer cell line. Int J Cancer 124:36-45
39. Hung CS, Peng YJ, Wei PL, Lee CH, Su HY, Ho YS, Lin SY, Wu CH, Chang YJ (2011) The alpha9 nicotinic acetylcholine receptor is the key mediator in nicotine-enhanced cancer metastasis in breast cancer cells. J Exp Clin Med 3:283-292
40. Han J, Goldstein LA, Gastman BR, Rabinowich H (2006) Interrelated roles for Mcl-1and BIM in regulation of TRAIL-mediated mitochondrial apoptosis. J Biol Chem 281:10153-101163
41. Zhou J, Wulfkuhle J, Zhang H, Gu P, Yang Y, Deng J, Margolick JB, Liotta LA, Petricoin E III, Zhang Y (2007) Activation of the PTEN/Mtor/STAT3 pathway in breast cancer stem-like cells in required for viability and maintenance. Proc Natl Acad Sci USA 104:16158-16163
42. Patrawala L, Calhoun T, Schneider-Broussard R, Zhou J, Claypool K, Tang DG (2005) Side population is enriched in tumorigenic, stem-like cancer cells, whereas ABCG2+ and ABCG2- cancer cells are similarly tumorigenic. Cancer Res 65:6207-6219
43. Hirschmann-Jax C, Foster AE, Wulf GG, Nuchtern JG, Jax TW, Gobel U, Goodell MA, Brenner MK (2004) A distinct "side population" of cells with druf efflux capacity in human tumor cells. Proc Natl Acad Sci USA 101:14228-14233
44. Zhou S, Schuetz JD, Bunting KD, Colapietro AM, Sampath J, Morris JJ, Lagutina I, Grosveld GC, Osawa M, Nakauchi H et al (2001) The ABC transporter Bcrp1/ABCG2 is expressed in wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat Med 7:1028-1034
45. George ZC, WeiZhou Z, Mei Sun QW, Domenico C, Mena M, LiMei X, Carliann C, Jin QC, Lu-Hai W (2008) Twist is transcriptionally induced by activation of STAT3 and mediates STAT3 oncogenic function. J Biol Chem 283:14665-14673
46. Ahmed H, Banerjee PP, Vasta GR (2007) Differential expression of galectins in normal, benign and malignant prostate epithelial cells: silencing of galectin-3 expression in prostate cancer by its promoter methylation. Biochem Biophys Res Commun 358:241-246
47. Alkondon M, Albuquerque EX (2004) The nicotinic acetylcholine receptor subtypes and their function in the hippocampus and cerebral cortex. Prog Brain Res 145:109-120
48. Arredondo J, Chernyavsky AI, Grando SA (2006) Nicotinic receptors mediate tumorigenic action of tobacco-derived nitrosamine on immortalized oral epithelial cells. Cancer Biol Ther 5:511-517
49. Wu CH, Lee CH, Ho YS (2011) Nicotinic acetylcholine receptor-based blockade: application of molecular targets for cancer therapy. Clin Cancer Res 17:3533-3541
50. Lee CH, Chang YC, Chen CS, Tu SH, Wang YJ, Chen LC, Chang YJ, Wei PL, Chang HW, Chang CH et al (2011) Crosstalk between nicotine and estrogen-induced estrogen receptor activation induces α9-nicotinic acetylcholine receptor expression in human breast cancer cells. Breast Cancer Res Treat 129:331-345
51. Chen RJ, Ho YS, Guo HR, Wang YJ (2008) Rapid activation of Stat3 and ERK1/2 by nicotine modulates cell proliferation in human bladder cancer cells. Toxicol Sci 104:283-293
52. Bowman T, Garcia R, Turkson J, Jove R (2000) STATs in oncogenesis. Oncogene 19:2474-2488
53. Real PJ, Sierra A, De Juan A, Segovia JC, Lopez-Vega JM, Fernandez-Luna JL (2002) Resistance to chemotherapy via Stat3-dependent overexpression of Bcl-2 in metastatic breast cancer cells. Oncogene 21:7611-7618
54. Mercer N, Ahmed H, Etcheverry SB, Vasta GR, Cortizo AM (2007) Regulation of advanced glycation end product (AGE) receptors and apoptosis by AGEs in osteoblast-like cells. Mol Cell Biochem 306:87-94
55. Ahmed H (2010) Promoter methylation in prostate cancer and its application for the early detection of prostate cancer using serum and urine samples. Biomark Cancer 2:17-33
56. Ahmed H, Guha P, Kaptan E, Bandyopadhyaya G (2011) Galectin-3: a potential target for cancer prevention. Trends Carbohydr Res 3:13-22
57. Fukumori T, Oka N, Takenaka Y, Nangia-Makker P, Elsamman E, Kasai T, Shono M, Kanayama HO, Ellerhors J, Lotan R et al (2006) Galectin-3 regulates mitochondrial stability and antiapoptotic function in response to anticancer drug in prostate cancer. Cancer Res 66:3114-3119
58. Hirata N, Sekino Y, Kanda Y (2010) Nicotine increases cancer stem cell population in MCF-7 cell. Biochem Biophys Res Commun 403:138-143
59. Zhang J, Kamdar O, Le W, Rosen GD, Upadhyay D (2009) Nicotine induces resistance to chemotherapy by modulating mitochondrial signaling in lung cancer. Am J Respir Cell Mol Biol 40:135-146
60. Shen T, Le W, Yee A, Kamdar O, Hwang PH, Upadhyay D (2010) Nicotine induces resistance to chemotherapy in nasal epithelial cancer. Am J Rhinol Allergy 24:73-77
61. An Y, Kiang A, Lopez JP, Kuo SZ, Yu MA, Abhold EL, Chen JS, Wang-Rodriguez J, Ongkeko WM (2012) Cigarette smoke promotes drug resistance and expansion of cancer stem cell-like side population. PLoS ONE 7:e47919