Skip to main content

Advertisement

SpringerLink
Log in

Increased mRNA expression of epidermal growth factor receptor, human epidermal receptor, and survivin in human gastric cancer after the surgical stress of laparotomy versus carbon dioxide pneumoperitoneum in a murine model

  • Published:
Surgical Endoscopy Aims and scope Submit manuscript

Abstract

Background

Surgical impact may be associated with enhanced tumor growth and chemoresistance. This study aimed to evaluate the effect of surgical impact on the mRNA expression of survivin, epidermal growth factor receptor (EGFR), and human epidermal receptor (HER2) in tumors after pneumoperitoneum versus laparotomy.

Methods

Nude mice were inoculated intraperitoneally with human gastric cancer cells (MKN45). Then laparotomy, carbon dioxide (CO2) pneumoperitoneum, and anesthesia alone were performed randomly, after which EGFR, HER2, and survivin mRNA expression using reverse transcription-polymerase chain reaction (RT-PCR) was evaluated.

Results

The expression of EGFR and HER2 mRNA increased significantly after the experiment. However, it was higher after laparotomy than after CO2 pneumoperitoneum at almost all examined time points. Survivin mRNA expression increased significantly in the first 48 h, then returned to the control level. It was higher after laparotomy than after CO2 pneumoperitoneum 48 h after the surgical procedures.

Conclusion

The expression of EGFR, HER2, and survivin increased after each surgical procedure. However it was lower after CO2 pneumoperitoneum than after laparotomy. This might be associated with changes in the chemosensitivity of the remnant cancer cells after surgery, supporting the use of minimally invasive surgery for cancer.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Yu W, Whang I, Suh I, Averbach A, Chang D, Sugarbaker PH (1998) Prospective randomized trial of early postoperative intraperitoneal chemotherapy as an adjuvant to resectable gastric cancer. Ann Surg 228:347–354

    Article  CAS  PubMed  Google Scholar 

  2. Han SW, Oh DY, Im SA, Park SR, Lee KW, Song HS, Lee NS, Lee KH, Choi IS, Lee MH, Kim MA, Kim WH, Bang YJ, Kim TY (2009) Phase II study and biomarker analysis of cetuximab combined with modified FOLFOX6 in advanced gastric cancer. Br J Cancer 100:298–304

    Article  CAS  PubMed  Google Scholar 

  3. Asanuma H, Torigoe T, Kamiguchi K, Hirohashi Y, Ohmura T, Hirata K, Sato M, Sato N (2005) Survivin expression is regulated by coexpression of human epidermal growth factor receptor 2 and epidermal growth factor receptor via phosphatidylinositol 3-kinase/AKT signaling pathway in breast cancer cells. Cancer Res 65:11018–11025

    Article  CAS  PubMed  Google Scholar 

  4. Jonker DJ, O’Callaghan CJ, Karapetis Cs, Zalcberg JR, Tu D, Au HJ, Berry SR, Krahn M, Price T, Simes RJ, Tebbutt NC, vanHazel G, Wiezbicki R, Langer C, Moore MJ (2007) Cetuximab for the treatment of colorectal cancer. N Engl J Med 357:2040–2048

    Article  CAS  PubMed  Google Scholar 

  5. Pinto C, Di Fabio F, Siena S, Cascinu S, Rojas Llimpe FL, Ceccarelli C, Mutri V, Gianetta L, Giaquinta S, Funaioli C, Berardi R, Longobardi C, Piana E, Martoni AA (2007) Phase II study of cetuximab in combination with FOLFIRI in patients with untreated advanced gastric or gastroesophageal junction adenocarcinoma (FULCETUX study). Ann Oncol 18:510–517

    Article  CAS  PubMed  Google Scholar 

  6. Coffey JC, Wang JH, Smith MJ, Laing A, Bouchier-Hayes D, Cotter TG, Redmond HP (2005) Phosphoinositide 3-kinase accelerates postoperative tumor growth by inhibiting apoptosis and enhancing resistance to chemotherapy-induced apoptosis. J Biol Chem 280:20968–20977

    Article  CAS  PubMed  Google Scholar 

  7. Lee SW, Gleason N, Blanco I, Asi ZK, Whelan RL (2002) Higher colon cancer tumor proliferative index and lower tumor cell death rate in mice undergoing laparotomy vs insufflation. Surg Endosc 16:36–39

    Article  CAS  PubMed  Google Scholar 

  8. Qadri SS, Wang JH, Coffey JC, Alam M, O’Donnell A, Aherne T, Redmond HP (2005) Surgically induced accelerated local and distant tumor growth is significantly attenuated by selective COX-2 inhibition. Ann Thorac Surg 79:990–995

    Article  PubMed  Google Scholar 

  9. Akiyama T, Sudo C, Ogawara H, Toyoshima K, Yamamoto T (1986) The product of the human c-erbB-2 gene: a 185-kilo Dalton glycoprotein with tyrosine kinase activity. Science 232:1644–1646

    Article  CAS  PubMed  Google Scholar 

  10. Gravalos C, Jimeno A (2008) HER2 in gastric cancer: a new prognostic factor and a novel therapeutic target. Ann Oncol 19:1523–1529

    Article  CAS  PubMed  Google Scholar 

  11. Altieri DC (2003) Validating survivin as a cancer therapeutic target. Nat Rev Cancer 3:46–54

    Article  CAS  PubMed  Google Scholar 

  12. Longlley DB, Johnston PG (2005) Molecular mechanisms of drug resistance. J Pathol 205:275–292

    Article  Google Scholar 

  13. Shin S, Sung BJ, Cho YS, Kim HJ, Ha NC, Hwang JI, Chung CW, Jung YK, Oh BH (2001) An anti-apoptotic protein human survivin is a direct inhibitor of caspase-3 and -7. Biochemistry 40:1117–1123

    Article  CAS  PubMed  Google Scholar 

  14. Wang Q, Greene MI (2005) EGFR enhances survivin expression through the phosphoinositide 3 (IP-3) kinase signaling pathway. Exp Mol Bathol 79:100–107

    Article  CAS  Google Scholar 

  15. Qiu L, Wang Q, Di W, Jiang Q, Schefeller E, Derby S, Wanebo H, Yan B, Wan Y (2005) Transient activation of EGFR/AKT pathway and expression of survivin contribute to reduced sensitivity of human melanoma cells to betulinic acid. Int J Oncol 27:823–830

    CAS  PubMed  Google Scholar 

  16. Peng XH, Cao ZH, Xia JT, Carlson GW, Lewis MM, Wood WC, Yang L (2005) Real-time detection of gene expression in cancer cells using molecular beacon imaging: new strategies for cancer research. Cancer Res 65:1909–1917

    Article  CAS  PubMed  Google Scholar 

  17. Ikeguchi M, Liu J, Kaibara N (2002) Expression of survivin mRNA and protein in gastric cancer cell line (MKN45) during cisplatin treatment. Apoptosis 7:23–29

    Article  CAS  PubMed  Google Scholar 

  18. Nakamura M, Tsuji N, Asanuma K, Kobayashi D, Yagihashi A, Hirata K, Torigoe T, Sato N, Watanabe N (2004) Survivin as a predictor of cis-diammine dichloroplatinum sensitivity in gastric cancer patients. Cancer Sci 95:44–51

    Article  CAS  PubMed  Google Scholar 

  19. Peng XH, Karna P, Cao Z, Jiang BH, Zhou M, Yang L (2006) Cross-talk between epidermal growth factor receptor and hypoxia inducible factor-1α signal pathways increase resistance to apoptosis by upregulating survivin gene expression. J Biol Chem 281:25903–25914

    Article  CAS  PubMed  Google Scholar 

  20. Matsui Y, Inomata M, Tojigamori M, Sonoda K, Shiraishi N, Kitano S (2005) Suppression of tumor growth in human gastric cancer with HER2 overexpression by an anti HER2 antobody in a murine model. Int J Oncol 27:681–685

    CAS  PubMed  Google Scholar 

  21. Suematsu T, Shiromizu A, Yamaguchi K, Shiraishi N, Adachi Y, Kitano S (1999) Convenient murine pneumoperitoneal model for the study of laparoscopic cancer surgery. Surg Laparo Endo Per 9:279–281

    Article  CAS  Google Scholar 

  22. Narita T, Taga T, Sugita K, Nakazawa S, Ohta S (2001) The autocrine loop of epidermal growth factor receptor–epidermal growth factor/transforming factor alpha in malignant rhabdoid tumor cell lines: heterogeneity of autocrine mechanism in TTC 549. Jpn J Cancer Res 92:269–278

    CAS  PubMed  Google Scholar 

  23. Revillion F, Hornez L, Peyrat JP (1997) Quuatification of c-erbB-2 gene expression in breast cancer by competitive RT-PCR. Clin Chem 43:2114–2120

    CAS  PubMed  Google Scholar 

  24. Zhang T, Fields JZ, Ehrlich SM (2004) The chemopreventive agent sulindac attenuates expression of the antiapoptotic protein survivin in colorectal carcinoma cells. J Pharmacol Exp Ther 308:434–437

    Article  CAS  PubMed  Google Scholar 

  25. Anwar TA, Shiraishi N, Ninomyia S, Tajima M, Inomata M, Kitano S (2009) Activation of nuclear factor kappa B (NFκB) and induction of migration inhibitory factor (MIF) in tumors by surgical stress of laparotomy vs CO2 pneumoperitoneum: an animal experiment. Surg Endosc. doi:10.1007/s00464-009-0609-x

  26. Abramovitch R, Marikovsky M, Meir G, Neeman M (1999) Stimulation of tumor growth by wound-derived growth factors. Br J Cancer 79:1392–1398

    Article  CAS  PubMed  Google Scholar 

  27. Rupec RA, Baeuerle PA (1995) The genomic response of tumor cells to hypoxia and reoxygenation: differential activation of transcription factors AP-1 and NFκB. Eur J Biochem 234:632–640

    Article  CAS  PubMed  Google Scholar 

  28. Lundberg O, Kristoffersson A (2005) Reduction of abdominal wall blood flow by clamping or carbon dioxide insufflation increases tumor growth in the abdominal wall: an experimental study in rats. Surg Endosc 19:720–723

    Article  CAS  PubMed  Google Scholar 

  29. Hsieh HL, Sun CC, Wu CB, Wu CY, Tung WH, Wang HH, Yang CM (2008) Sphnigosine 1-phosphate induces EGFR expression via Akt/NFκB and ERK/Ap-1 pathways in rat vascular smooth muscle cells. J Cell Biochem 103:1732–1746

    Article  CAS  PubMed  Google Scholar 

  30. Islam A, Kageyama H, Takada N, Kawamoto T, Takayasu H, Isogai E, Ohira M, Hashizume K, Kobayashi H, Kaneko Y, Nakagawara A (2000) High expression of survivin, mapped to 17q25, is significantly associated with poor prognostic factors and promotes cell survival in human neuroblastoma. Oncogene 19:617–623

    Article  CAS  PubMed  Google Scholar 

  31. Kawasaki H, Altieri DC, Lu CD, Toyoda M, Tenjo T, Tanigawa N (1998) Inhibition of apoptosis by survivin predicts shorter survival rates in colorectal cancer. Cancer Res 58:5071–5074

    CAS  PubMed  Google Scholar 

  32. Mayo SC, Austin DF, Sheppard BC, Mori M, Shipley DK, Billingsley KG (2009) Evolving preoperative evaluation of patients with pancreatic cancer: does laparoscopy have a role in the current era. J Am Coll Surg 208:87–95

    Article  PubMed  Google Scholar 

  33. Tagliabue E, Agresti R, Carcangiu ML, Ghirelli C, Morelli D, Campiglio M, Martel M, Giovanazzi R, Greco M, Balsari A, Menard S (2003) Role of HER2 in wound induced breast carcinoma proliferation. Lancet 362:527–533

    Article  CAS  PubMed  Google Scholar 

  34. Jarnagin WR, Delman K, Kooby D, Mastorides S, Zager J, Brennan MF, Blumgart LH, Federoff H, Fong Y (2000) Neoadjuvant interleukin-12 immunogene therapy protects against cancer recurrence after liver resection in an animal model. Ann Surg 231:762–771

    Article  CAS  PubMed  Google Scholar 

  35. Wei JM, Shiraishi N, Goto S, Yasuda K, Inomata M, Kitano S (2008) Laparoscopy-assisted distal gastrectomy with D1 + β compared with D1α lymph node dissection. Surg Endosc 22:955–960

    Article  PubMed  Google Scholar 

Download references

Acknowledgment

This work was supported in part by a Grant-in-Aid for Scientific Research (no. 050916) from the Ministry of Education, Science, Culture, and Sports, Japan.

Disclosures

Anwar Tawfik Amin, Norio Shiraishi, Shigeo Ninomiya, Masaaki Tajima, Masafumi Inomata, and Seigo Kitano have no conflict of interest or financial ties to disclose.

Author information

Authors and Affiliations

  1. Department of Gastroenterological Surgery, Oita University Faculty of Medicine, 1-1 Idaigaoka, Yufu, Oita, 879-5593, Japan

    Anwar Tawfik Amin, Norio Shiraishi, Shigeo Ninomiya, Masaaki Tajima, Masafumi Inomata & Seigo Kitano

  2. South Egypt Cancer Institute, Surgery Department, Assiut University, Assiut, Egypt

    Anwar Tawfik Amin

Authors
  1. Anwar Tawfik Amin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Norio Shiraishi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shigeo Ninomiya
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Masaaki Tajima
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Masafumi Inomata
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Seigo Kitano
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anwar Tawfik Amin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Amin, A.T., Shiraishi, N., Ninomiya, S. et al. Increased mRNA expression of epidermal growth factor receptor, human epidermal receptor, and survivin in human gastric cancer after the surgical stress of laparotomy versus carbon dioxide pneumoperitoneum in a murine model. Surg Endosc 24, 1427–1433 (2010). https://doi.org/10.1007/s00464-009-0793-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00464-009-0793-8

Keywords

Search

Navigation