Single-Cell Analysis Reveals Early Manifestation of Cancerous Phenotype in Pre-Malignant Esophageal Cells

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Wang, Jiangxin ^a   Shi, Xu ^a   Johnson, Roger H ^a   Kelbauskas, Laimonas ^a   Zhang, Weiwen ^a,b   Meldrum, Deirdre R ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b TIANJIN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; MITOCHONDRIAL DNA;

ARTICLE; BARRETT ESOPHAGUS; CELL HETEROGENEITY; CELL HYPOXIA; CELL STRESS; CONTROLLED STUDY; COPY NUMBER VARIATION; DISEASE COURSE; ESOPHAGUS CANCER; ESOPHAGUS DYSPLASIA; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; METAPLASIA; MITOCHONDRIAL GENE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; NUCLEAR GENE; PATHOGENESIS; PHENOTYPE; PRECANCER; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SINGLE CELL ANALYSIS;

EID: 84885147424     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075365     Document Type: Article

References (73)

1. Chen XX, Yang CS, (2001) Esophageal adenocarcinoma: a review and perspectives on the mechanism of carcinogenesis and chemoprevention. Carcinogenesis 22: 1119-1129.
2. Chen G, Izzo J, Demizu Y, Wang F, Guha S, et al. (2009) Different redox states in malignant and nonmalignant esophageal epithelial cells and differential cytotoxic responses to bile acid and honokiol. Antioxid Redox Signal 11: 1083-1095.
3. Barrett MT, Pritchard D, Palanca-Wessels C, Anderson J, Reid BJ, et al. (2003) Molecular phenotype of spontaneously arising 4N (G2-Tetraploid) intermediates of neoplastic progression in Barrett's esophagus. Cancer Res 63: 4211-4217.
4. Coco D, Srivastava A, Sanchez C, Fong PY, Li X, et al. (2011) Mitoses, genomic instability and neoplastic progression in Barrett's esophagus. Lab Invest 91: 145A-146A.
5. McIntire M, Sanchez CA, Cowan DS, Reid B, Fong PY, et al. (2011) Role of inflammation in Barrett's esophagus-related cancer development. Lab Invest 91: 159A-159A.
6. Reid BJ, Kostadinov R, Maley CC, (2011) New strategies in Barrett's esophagus: Integrating clonal evolutionary theory with clinical management. Clin Cancer Res 17: 3512-3519.
7. Olliver JR, Hardie LJ, Gong YY, Dexter S, Chalmers D, et al. (2005) DNA damage, risk factors, and disease progression in Barrett's oesophagus. Gut 54: A51-A52.
8. Wang S, Zhan M, Yin J, Abraham JM, Mori Y, et al. (2006) Transcriptional profiling suggests that Barrett's metaplasia is an early intermediate stage in esophageal adenocarcinogenesis. Oncogene 25: 3346-3356.
9. Brahimi-Horn MC, Bellot G, Pouysségur J, (2011) Hypoxia and energetic tumour metabolism. Current Opinion in Genetics & Development 21: 67-72.
10. Cosse J-P, Michiels C, (2008) Tumour Hypoxia affects the responsiveness of cancer cells to chemotherapy and promotes cancer progression. Anti-Cancer Agents in Medicinal Chemistry (Formerly Current Medicinal Chemistry) 8: 790-797.
11. Heddleston JM, Li Z, Lathia JD, Bao S, Hjelmeland AB, et al. (2010) Hypoxia inducible factors in cancer stem cells. Br J Cancer 102: 789-795.
12. Koi M, Boland CR, (2011) Tumor hypoxia and genetic alterations in sporadic cancers. Journal of Obstetrics and Gynaecology Research 37: 85-98.
13. Nordgren IK, Tavassoli A, (2011) Targeting tumour angiogenesis with small molecule inhibitors of hypoxia inducible factor. Chem Soc Rev 40: 4307-4317.
14. Yang Y, Sun M, Wang L, Jiao B, (2013) HIFs, angiogenesis, and cancer. Journal of Cellular Biochemistry 114: 967-974.
15. Tang C-M, Yu J, (2013) Hypoxia-inducible factor-1 as a therapeutic target in cancer. Journal of Gastroenterology and Hepatology 28: 401-405.
16. Bertout JA, Patel SA, Simon MC, (2008) The impact of O2 availability on human cancer. Nat Rev Cancer 8: 967-975.
17. Yu M, (2011) Generation, function and diagnostic value of mitochondrial DNA copy number alterations in human cancers. Life Sci 89: 65-71.
18. Clay Montier LL, Deng JJ, Bai Y, (2009) Number matters: control of mammalian mitochondrial DNA copy number. Journal of Genetics and Genomics 36: 125-131.
19. Wang GC, Hazra TK, Mitra S, Lee HM, Englander EW, (2000) Mitochondrial DNA damage and a hypoxic response are induced by CoCI2 in rat neuronal PC12 cells. Nucleic Acids Res 28: 2135-2140.
20. Elowitz MB, Levine AJ, Siggia ED, Swain PS, (2002) Stochastic gene expression in a single cell. Science 297: 1183-1186.
21. Raj A, van Oudenaarden A, (2008) Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 135: 216-226.
22. Lidstrom ME, Meldrum DR, (2003) Life-on-a-chip. Nat Rev Microbiol 1: 158-164.
23. Huang HM, Fowler C, Zhang H, Gibson GE, (2004) Mitochondrial heterogeneity within and between different cell types. Neurochem Res 29: 651-658.
24. Cree LM, Patel SK, Pyle A, Lynn S, Turnbull DM, et al. (2008) Age-related decline in mitochondrial DNA copy number in isolated human pancreatic islets. Diabetologia 51: 1440-1443.
25. Kuznetsov AV, Margreiter R, (2009) Heterogeneity of mitochondria and mitochondrial function within cells as another level of mitochondrial complexity. Int J Mol Sci 10: 1911-1929.
26. Longo D, Hasty J, (2006) Dynamics of single-cell gene expression. Mol Syst Biol 2: 64.
27. Axelson H, Fredlund E, Ovenberger M, Landberg G, Pahlman S, (2005) Hypoxia-induced dedifferentiation of tumor cells- A mechanism behind heterogeneity and aggressiveness of solid tumors. Semin Cell Dev Biol 16: 554-563.
28. Bengtsson M, Hemberg M, Rorsman P, Stahlberg A, (2008) Quantification of mRNA in single cells and modelling of RT-qPCR induced noise. BMC Mol Biol 9: 63.
29. Taniguchi K, Kajiyama T, Kambara H, (2009) Quantitative analysis of gene expression in a single cell by qPCR. Nat Methods 6: 503-506.
30. Li Y, Thompson H, Hemphill C, Hong F, Forrester J, et al. (2010) An improved one-tube RT-PCR protocol for analyzing single-cell gene expression in individual mammalian cells. Anal Bioanal Chem 397: 1853-1859.
31. Zeng J, Wang J, Gao W, Mohammadreza A, Kelbauskas L, et al. (2011) Quantitative single-cell gene expression measurements of multiple genes in response to hypoxia treatment. Anal Bioanal Chem 401: 3-13.
32. Palanca-Wessels MC, Barrett MT, Galipeau PC, Rohrer KL, Reid BJ, et al. (1998) Genetic analysis of long-term Barrett's esophagus epithelial cultures exhibiting cytogenetic and ploidy abnormalities. Gastroenterology 114: 295-304.
33. Torres-Garcia W, Ashili S, Kelbauskas L, Johnson RH, Zhang W, et al. (2012) A statistical framework for multiparameter analysis at the single-cell level. Mol Biosyst 8: 804-817.
34. Zhu H, Holl M, Ray T, Bhushan S, Meldrum DR (2009) Characterization of deep wet etching of fused silica glass for single cell and optical sensor deposition. J Micromech Microeng 19.
35. Kelbauskas L, Ashili SP, Houkal J, Smith D, Mohammadreza A, et al. (2012) Method for physiologic phenotype characterization at the single-cell level in non-interacting and interacting cells. J Biomed Opt 17.
36. Anis Y, Holl M, Meldrum D, (2010) Automated selection and placement of single cells using vision-based feedback control. IEEE Transactions on Automation Science and Engineering 7: 598-606.
37. Ashili SP, Kelbauskas L, Houkal J, Smith D, Tian Y, et al. (2011) Automated platform for multiparameter stimulus response studies of metabolic activity at the single-cell level, Proceedings Vol.7929, Microfluidics, BIOMEMS, and Medical Microsystems IX, 2011.
38. Yoshiji H, Gomez DE, Shibuya M, Thorgeirsson UP, (1996) Expression of vascular endothelial growth factor, its receptor, and other angiogenic factors in human breast cancer. Cancer Res 56: 2013-2016.
39. Matarrese P, Testa U, Cauda R, Vella S, Gambardella L, et al. (2001) Expression of P-170 glycoprotein sensitizes lymphoblastoid CEM cells to mitochondria-mediated apoptosis. Biochem J 355: 587-595.
40. St John JC, Amaral A, Bowles E, Oliveira JF, Lloyd R, et al. (2006) The analysis of mitochondria and mitochondrial DNA in human embryonic stem cells. Methods Mol Biol 331: 347-374.
41. Liu T, Hannafon B, Gill L, Kelly W, Benbrook D, (2007) Flex-Hets differentially normal cells by directly induce apoptosis in cancer over targeting mitochondria. Mol Cancer Ther 6: 1814-1822.
42. Gao W, Zhang W, Meldrum DR, (2011) RT-qPCR based quantitative analysis of gene expression in single bacterial cells. J Microbiol Methods 85: 221-227.
43. Alonso A, Martin P, Albarran C, Garcia P, Garcia O, et al. (2004) Real-time PCR designs to estimate nuclear and mitochondrial DNA copy number in forensic and ancient DNA studies. Forensic SciInt 139: 141-149.
44. Kadowaki T, Kitagawa Y, (1991) Hypoxic depression of mitochondrial mRNA levels in HeLa cell. Exp Cell Res 192: 243-247.
45. Brouwer M, Brown-Peterson NJ, Hoexum-Brouwer T, Manning S, Denslow N, (2008) Changes in mitochondrial gene and protein expression in grass shrimp, Palaemonetes pugio, exposed to chronic hypoxia. Mar Environ Res 66: 143-145.
46. Wang B, Wood IS, Trayhurn P, (2008) PCR arrays identify metallothionein-3 as a highly hypoxia-inducible gene in human adipocytes. Biochem Biophys Res Commun 368: 88-93.
47. Murata M, Yudo K, Nakamura H, Chiha J, Okamoto K, et al. (2009) Hypoxia upregulates the expression of angiopoietin-Like-4 in human articular chondrocytes: Role of angiopoietin-Like-4 in the expression of matrix metalloproteinases and cartilage degradation. J Orthop Res 27: 50-57.
48. Lee JJ, Natsuizaka M, Ohashi S, Wong GS, Takaoka M, et al. (2010) Hypoxia activates the cyclooxygenase-2-prostaglandin E synthase axis. Carcinogenesis 31: 427-434.
49. Zamzami N, Marchetti P, Castedo M, Decaudin D, Macho A, et al. (1995) Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell-death. J Exp Med 182: 367-377.
50. Moro L, Arbini AA, Marra E, Greco M, (2008) Mitochondrial DNA depletion reduces PARP-1 levels and promotes progression of the neoplastic phenotype in prostate carcinoma. Analytical Cellular Pathology 30: 307-322.
51. Yu M, Zhou Y, Shi Y, Ning L, Yang Y, et al. (2007) Reduced mitochondrial DNA copy number is correlated with tumor progression and prognosis in Chinese breast cancer patients. IUBMB Life 59: 450-457.
52. Wang Y, Liu VWS, Xue WC, Cheung ANY, Ngan HYS, (2006) Association of decreased mitochondrial DNA content with ovarian cancer progression. Br J Cancer 95: 1087-1091.
53. Mizumachi T, Muskhelishvili L, Naito A, Furusawa J, Fan C-Y, et al. (2008) Increased distributional variance of mitochondrial DNA content associated with prostate cancer cells as compared with normal prostate cells. The Prostate 68: 408-417.
54. Jones JB, Song JJ, Hempen PM, Parmigiani G, Hruban RH, et al. (2001) Detection of Mitochondrial DNA Mutations in Pancreatic Cancer Offers a "Mass"-ive Advantage over Detection of Nuclear DNA Mutations. Cancer Res 61: 1299-1304.
55. Penta JS, Johnson FM, Wachsman JT, Copeland WC, (2001) Mitochondrial DNA in human malignancy. Mutat Res-Rev Mutat Res 488: 119-133.
56. Yang H, (2011) Correlation between increased copy number of mitochondrial DNA and clinicopathological stage in colorectal cancer. Oncology Letters 2: 899-903.
57. Shapovalov Y, Hoffman D, Zuch D, Bentley KL de M, Elisee RA, (2011) Mitochondrial dysfunction in cancer cells due to aberrant mitochondrial replication. J Biol Chem 286: 22331-22338.
58. Thyagarajan B, Wang R, Nelson H, Barcelo H, Koh W-P, et al. (2013) Mitochondrial DNA copy number is associated with breast cancer risk. PLoS ONE 8: e65968.
59. Cormio A, Guerra F, Cormio G, Pesce V, Fracasso F, et al. (2012) Mitochondrial DNA content and mass increase in progression from normal to hyperplastic to cancer endometrium. BMC Research Notes 5: 279.
60. Kim MM, Clinger JD, Masayesva BG, Ha PK, Zahurak ML, et al. (2004) Mitochondrial DNA quantity increases with histopathologic grade in premalignant and malignant head and neck lesions. Clin Cancer Res 10: 8512-8515.
61. Lin C-S, Chang S-C, Wang L-S, Chou T-Y, Hsu W-H, et al. (2010) The role of mitochondrial DNA alterations in esophageal squamous cell carcinomas. The Journal of Thoracic and Cardiovascular Surgery 139: 189-197.e4.
62. Fukuda R, Zhang H, Kim J, Shimoda L, Dang CV, et al. (2007) HIF-1 regulates cytochrome oxidase subunits to optimize efficiency of respiration in hypoxic cells. Cell 129: 111-122.
63. Semenza GL, (2011) Hypoxia-inducible factor 1: Regulator of mitochondrial metabolism and mediator of ischemic preconditioning. Biochim Biophys Acta-Mol Cell Res 1813: 1263-1268.
64. Hochachka PW, Buck LT, Doll CJ, Land SC, (1996) Unifying theory of hypoxia tolerance: Molecular metabolic defense and rescue mechanisms for surviving oxygen lack. Proc Natl Acad Sci USA 93: 9493-9498.
65. Davis S, Weiss M, Wong J, Lampidis T, Chen L, (1985) Mitochondrial and plasma-membrane potentials cause unusual accumulation and retention of Rhodamine-123 by Human-Breast adenocarcinoma-derived Mcf-7 cells. J Biol Chem 260: 3844-3850.
66. Heerdt BG, Houston NA, Augenlicht LH, (2006) Growth properties of colonic tumor cells are a function of the intrinsic mitochondrial membrane potential. Cancer Res 66: 1591-1596.
67. Houston MA, Augenlicht LH, Heerdt BG, (2011) Intrinsic mitochondrial membrane potential and associated tumor phenotype are independent of MUC1 over-expression. PLoS One 6: e25207.
68. Klohn PC, Soriano ME, Irwin W, Penzo D, Scorrano L, et al. (2003) Early resistance to cell death and to onset of the mitochondrial permeability transition during hepatocarcinogenesis with 2-acetylaminofluorene. Proc Natl Acad Sci USA 100: 10014-10019.
69. Solaini G, Sgarbi G, Baracca A, (2011) Oxidative phosphorylation in cancer cells. Biochim Biophys Acta-Bioenerg 1807: 534-542.
70. Garciahorsman J, Barquera B, Rumbley J, Ma J, Gennis R, (1994) The superfamily of Heme-Copper respiratory oxidases. J Bacteriol 176: 5587-5600.
71. Boettiger AN, Ralph PL, Evans SN, (2011) Transcriptional regulation: Effects of promoter proximal pausing on speed, synchrony and reliability. PLoS Comput Biol 7: e1001136.
72. Munsky B, Neuert G, van Oudenaarden A, (2012) Using gene expression noise to understand gene regulation. Science 336: 183-187.
73. Raj A, van Oudenaarden A, (2009) Single-Molecule approaches to stochastic gene expression. Annual Review of Biophysics. Palo Alto: Annual Reviews 38: 255-270.