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Identification of Differentially Expressed Genes in Lung Tissues of Nickel-Exposed Rats Using Suppression Subtractive Hybridization

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Abstract

Occupational exposure to nickel compound, such as nickel refining, electroplating, and in conjunction with other metals, is harmful to the health, causing respiratory distress, and lung and nasal cancer. In this work, the different gene expression patterns of lung tissues from nickel-exposed rats and controls were investigated. The suppression subtractive hybridization (SSH) method was used to generate two subtracted cDNA libraries with gene transcripts differentially expressed after nickel inducing. Dot-blot hybridizations were used to confirm differential ratios of expression of obtained SSH clones. Out of 768 unique SSH clones, which were chosen randomly from the two subtraction libraries (384 of each), 319 could be verified as differentially expressed. According to blast screening and functional annotation, 28% genes in nickel-induced cDNA library were related to cell differentiation, whereas 21% in driver library were related to oxygen transport. Two novel expressed sequence tags (ESTs; NCBI Accession No. FC809414 and No. FC809411) in nickel-induced cDNA library were obtained. The genes detected in the present study are probably important genes associated with nickel-induced lung cancer.

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References

  1. Bennett BG (1984) Environmental nickel pathways to man. IARC Sci Publ 53:487–495

    PubMed  CAS  Google Scholar 

  2. Grandjean P (1984) Human exposure to nickel. IARC Sci Publ: 469–485

  3. Doll R (1984) Nickel exposure: a human health hazard. IARC Sci Publ: 3–21

  4. IARC International Agency for Research on Cancer (1990) Chromium, nickel and welding. IARC Monogr Eval Carcinog Risks Hum 49:1–648

    Google Scholar 

  5. Kasprzak KS, Sunderman FW Jr, Salnikow K (2003) Nickel carcinogenesis. Mutat Res 533:67–97

    Article  PubMed  CAS  Google Scholar 

  6. Salnikow K, Gao M, Voitkun V et al (1994) Altered oxidative stress responses in nickel-resistant mammalian-cells. Cancer Res 54:6407–6412

    PubMed  CAS  Google Scholar 

  7. Zhou DJ, Salnikow K, Costa M (1998) Cap43, a novel gene specifically induced by Ni2+ compounds. Cancer Res 58:2182–2189

    PubMed  CAS  Google Scholar 

  8. Smith JB, Smith L, Pijuan V et al (1994) Transmembrane signals and protooncogene induction evoked by carcinogenic metals and prevented by zinc. Environ Health Perspect 102(Suppl 3):181–189

    Article  PubMed  CAS  Google Scholar 

  9. Li Q, Suen TC, Sun H et al (2009) Nickel compounds induce apoptosis in human bronchial epithelial Beas-2B cells by activation of c-Myc through ERK pathway. Toxicol Appl Pharmacol 235:191–198

    Article  PubMed  CAS  Google Scholar 

  10. Higinbotham KG, Rice JM, Diwan BA et al (1992) GGT to GTT transversions in codon 12 of the K-ras oncogene in rat renal sarcomas induced with nickel subsulfide or nickel subsulfide/iron are consistent with oxidative damage to DNA. Cancer Res 52:4747–4751

    PubMed  CAS  Google Scholar 

  11. Denkhaus E, Salnikow K (2002) Nickel essentiality, toxicity, and carcinogenicity. Crit Rev Oncol Hematol 42:35–56

    Article  PubMed  CAS  Google Scholar 

  12. Kowara R, Karaczyn A, Cheng RY et al (2005) Microarray analysis of altered gene expression in murine fibroblasts transformed by nickel(II) to nickel(II)-resistant malignant phenotype. Toxicol Appl Pharmacol 205:1–10

    Article  PubMed  CAS  Google Scholar 

  13. Cheng RY, Zhao A, Alvord WG et al (2003) Gene expression dose-response changes in microarrays after exposure of human peripheral lung epithelial cells to nickel(II). Toxicol Appl Pharmacol 191:22–39

    Article  PubMed  CAS  Google Scholar 

  14. Ohmori T, Okada K, Terada M et al (1999) Low susceptibility of specific inbred colonies of rats to nickel tumorigenesis in soft tissue. Cancer Lett 136:53–58

    Article  PubMed  CAS  Google Scholar 

  15. Bermudez Y, Yang H, Cheng JQ et al (2008) Pyk2/ERK 1/2 mediate Spl- and c-Myc-dependent induction of telomerase activity by epidermal growth factor. Growth Factors 26:1–11

    Article  PubMed  CAS  Google Scholar 

  16. Ahmed NN, Grimes HL, Bellacosa A et al (1997) Transduction of interleukin-2 antiapoptotic and proliferative signals via Akt protein kinase. Proc Natl Acad Sci USA 94:3627–3632

    Article  PubMed  CAS  Google Scholar 

  17. Suer S, Sonmez H, Karaaslan I et al (1996) Tissue sialic acid and fibronectin levels in human prostatic cancer. Cancer Lett 99:135–137

    Article  PubMed  CAS  Google Scholar 

  18. Helle SI (2004) The insulin-like growth factor system in advanced breast cancer. Best Pract Res Clin Endocrinol Metab 18:67–79

    Article  PubMed  CAS  Google Scholar 

  19. Daly RJ, Harris WH, Wang DY et al (1991) Autocrine production of insulin-like growth factor II using an inducible expression system results in reduced estrogen sensitivity of MCF-7 human breast cancer cells. Cell Growth Differ 2:457–464

    PubMed  CAS  Google Scholar 

  20. Ellis MJ, Leav BA, Yang Z et al (1996) Affinity for the insulin-like growth factor-II (IGF-II) receptor inhibits autocrine IGF-II activity in MCF-7 breast cancer cells. Mol Endocrinol 10:286–297

    Article  PubMed  CAS  Google Scholar 

  21. Chiang WL, Chu SC, Yang SS et al (2002) The aberrant expression of cytosolic carbonic anhydrase and its clinical significance in human non-small cell lung cancer. Cancer Lett 188:199–205

    Article  PubMed  CAS  Google Scholar 

  22. Chegwidden WR, Dodgson SJ, Spencer IM (2000) The roles of carbonic anhydrase in metabolism, cell growth and cancer in animals. EXS 90:343–363

    PubMed  CAS  Google Scholar 

  23. Crandall ED, O’Brasky JE (1978) Direct evidence of participation of rat lung carbonic anhydrase in CO2 reactions. J Clin Invest 62:618–622

    Article  PubMed  CAS  Google Scholar 

  24. Enns T, Hill EP (1983) CO2 diffusing capacity in isolated dog lung lobes and the role of carbonic anhydrase. J Appl Physiol 54:483–490

    PubMed  CAS  Google Scholar 

  25. Wykoff CC, Beasley NJ, Watson PH et al (2000) Hypoxia-inducible expression of tumor-associated carbonic anhydrases. Cancer Res 60:7075–7083

    PubMed  CAS  Google Scholar 

  26. Sherwood BT, Colquhoun AJ, Richardson D et al (2007) Carbonic anhydrase IX expression and outcome after radiotherapy for muscle-invasive bladder cancer. Clin Oncol (R Coll Radiol) 19:777–783

    Article  CAS  Google Scholar 

  27. Salnikow K, An WG, Melillo G et al (1999) Nickel-induced transformation shifts the balance between HIF-1 and p53 transcription factors. Carcinogenesis 20:1819–1823

    Article  PubMed  CAS  Google Scholar 

  28. Williams AS, Eynott PR, Leung SY et al (2009) Role of cathepsin S in ozone-induced airway hyperresponsiveness and inflammation. Pulm Pharmacol Ther 22:27–32

    Article  PubMed  CAS  Google Scholar 

  29. Wozniak MA, Modzelewska K, Kwong L et al (2004) Focal adhesion regulation of cell behavior. Biochim Biophys Acta 1692:103–119

    Article  PubMed  CAS  Google Scholar 

  30. Karmakar S, Mukherjee R (2003) Integrin receptors and ECM proteins involved in preferential adhesion of colon carcinoma cells to lung cells. Cancer Lett 196:217–227

    Article  PubMed  CAS  Google Scholar 

  31. Sjodin A, Guo DS, Sorhaug S et al (2003) Dysregulated secretoglobin expression in human lung cancers. Lung Cancer 41:49–56

    Article  PubMed  Google Scholar 

  32. Wang L, Liu R, Chi Z et al (2010) Spectroscopic investigation on the toxic interactions of Ni2+ with bovine hemoglobin. Spectrochim Acta A Mol Biomol Spectrosc 76:155–160

    Article  PubMed  Google Scholar 

  33. Scheller FW, Bistolas N, Liu S et al (2005) Thirty years of haemoglobin electrochemistry. Adv Colloid Interface Sci 116:111–120

    Article  PubMed  CAS  Google Scholar 

  34. Goldberg MA, Dunning SP, Bunn HF (1988) Regulation of the erythropoietin gene: evidence that the oxygen sensor is a heme protein. Science 242:1412–1415

    Article  PubMed  CAS  Google Scholar 

  35. Shibayama N, Morimoto H, Kitagawa T (1986) Properties of chemically modified Ni(II)-Fe(II) hybrid hemoglobins. Ni(II) protoporphyrin IX as a model for a permanent deoxy-heme. J Mol Biol 192:331–336

    Article  PubMed  CAS  Google Scholar 

  36. Martinez-Tabche L, Mora BR, Olivan LG et al (1999) Toxic effect of nickel on hemoglobin concentration of Limnodrilus hoffmeisteri in spiked sediments of trout farms. Ecotoxicol Environ Saf 42:143–149

    Article  PubMed  CAS  Google Scholar 

  37. Yang MC, Guo Y, Liu CC et al (2006) The TTF-1/TAP26 complex differentially modulates surfactant protein-B (SP-B) and -C (SP-C) promoters in lung cells. Biochem Biophys Res Commun 344:484–490

    Article  PubMed  CAS  Google Scholar 

  38. Rocks N, Paulissen G, El Hour M et al (2008) Emerging roles of ADAM and ADAMTS metalloproteinases in cancer. Biochimie 90:369–379

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This research was supported by Natural Science Foundation of China (30570690, 81041069) and the Natural Science Foundation of Shanghai (08ZR1420700).

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Authors and Affiliations

  1. School of Life Science and Technology, Tongji University, Shanghai, 200092, China

    Jing Zhang, Lihong Liu, Mengjie Li & Ying Wang

  2. Department of Regenerative Medicine, Tongji University Scholl of Medicine, Shanghai, 200092, China

    Jun Zhang, Yingying Fan, Yang Zhou, Zhihua Shao & Hongjun Shi

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  1. Jing Zhang
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  2. Jun Zhang
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  3. Yingying Fan
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  4. Lihong Liu
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  5. Mengjie Li
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  6. Yang Zhou
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  7. Zhihua Shao
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  8. Hongjun Shi
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  9. Ying Wang
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Correspondence to Jun Zhang.

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Jing Zhang and Jun Zhang contributed equally to this work.

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Zhang, J., Zhang, J., Fan, Y. et al. Identification of Differentially Expressed Genes in Lung Tissues of Nickel-Exposed Rats Using Suppression Subtractive Hybridization. Biol Trace Elem Res 143, 1007–1017 (2011). https://doi.org/10.1007/s12011-010-8898-4

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  • DOI: https://doi.org/10.1007/s12011-010-8898-4

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