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Effect of CO2 pneumoperitoneum on the proliferation of human ovarian cancer cell line SKOV-3 and the expression of NM23-H1 and MMP-2

  • Gynecologic Oncology
  • Published:
Archives of Gynecology and Obstetrics Aims and scope Submit manuscript

Abstract

Objective

This study aims to investigate the impacts of CO2 pneumoperitoneum on the growth of ovarian cancer in nude mice and the expression of tumor metastasis suppressor gene (NM23-H1) and matrix metalloproteinase -2 (MMP-2) in SKOV-3 ovarian cancer cell line cancer tissue.

Method

Forty five  nude mice were used to establish ovarian cancer xenograft models by intraperitoneal injection of human ovarian cancer cell line SKOV-3. Murine xenograft models were divided into four groups: control group (only anesthetized for 0.5 h), laparotomy group (laparotomy for 0.5 h), CO2 pneumoperitoneum of 0.5 h, and CO2 pneumoperitoneum of 1 h group. Mice were killed after 12 weeks to observe intraperitoneal tumor growth and detected mRNA expression of NM23-H1 and MMP-2 in tumor tissues by RT-PCR.

Result

Our data show that xenograft tumors grew faster in the CO2 pneumoperitoneum groups than that in control and laparotomy groups and even faster in the CO2 pneumoperitoneum of 1 h group. The mRNA expression of NM23-H1 in CO2 pneumoperitoneum groups was significantly lower than that in control group and laparotomy group (P < 0.01). Moreover, the longer duration of CO2 pneumoperitoneum negatively correlated with lower expression of NM23-H1 (P < 0.01). In contrast to NM23-H1, MMP-2 expression was significantly higher in CO2 pneumoperitoneum groups than that in the control group and laparotomy group (P < 0.01) and positively correlated with the duration of CO2 pneumoperitoneum (P < 0.01). In addition, there was a negative correlation between the expression of NM23-H1 and MMP-2 (r = –0.984, P < 0.05).

Conclusion

The CO2 pneumoperitoneum could promote the proliferation and metastasis of human ovarian cancer in nude mice. This effect was positively correlated with the duration of CO2 pneumoperitoneum.

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References

  1. Nezhat C, Luciano A, Siegler A, Nezhat F, Nezhat C, Seldman D (2000) Operative gynecologic laparoscopy; principles and techniques, 2nd edn. McGraw Hill, New York

    Google Scholar 

  2. Dobronte Z, Wittmann T, Karacsony G (1978) Rapid development of malignant metastesis in the abdominal wall after laparoscopy. Endoscopy 10:127–130

    Article  CAS  PubMed  Google Scholar 

  3. Paolucci V, Schaeff B, Schneider M, Gutt C (1999) Tumor seeding following laparoscopy: international Survey. World J Surg 23:989–995

    Article  CAS  PubMed  Google Scholar 

  4. Martinez J, Targarona EM, Balagué C, Pera M, Trias M (1995) Port site metastasis. An unresolved problem in laparoscopic surgery. A review. Int Surg 80:315–321

    CAS  PubMed  Google Scholar 

  5. Wittich P, Steyerberg ER, Simons SH, Marquet RL, Bonjer HJ (2000) Intraperitoneal tumor growth is influenced by pressure of carbon dioxide pneumoperitoneum. Surg Endosc 14:817–819

    Article  CAS  PubMed  Google Scholar 

  6. Yokoyama M, Ishida H, Okita T, Murata N, Hashimoto D (2003) Oncological effects of insufflation with different gases and gasless procedure in rats. Surg Endose 17:1151–1155

    Article  CAS  Google Scholar 

  7. Bergström M, Falk P, Park PO, Holmdahl L (2008) Peritoneal and systemic pH during pneumoperitoneum with CO2 and helium in a pig model. Surg Endosc 22:359–364

    Article  PubMed  Google Scholar 

  8. Kuntz C, Wunsch A, Bödeker C, Bay F, Rosch R, Windeler J, Herfarth C (2000) Effect of pressure and gas type on intraabdominal, subcutaneous, and blood pH in laparoscopy. Surg Endosc 14:367–371

    Article  CAS  PubMed  Google Scholar 

  9. Kim ZG, Mehl C, Lorenz M, Gutt CN (2002) Impact of laparoscopic CO2 insufflation on tumor associated molecules in cultured colorectal cancer cells. Surg Endosc 16:1182–1186

    Article  CAS  PubMed  Google Scholar 

  10. Ziprin P, Ridgway PF, Peck DH, Darzi AW (2003) Laparoscopic enhancement of tumor cell binding to the peritoneum is inhibited by anti-intercellular adhesion molecule monoclonal antibody. Surg Endosc 17:1812–1817

    Article  CAS  PubMed  Google Scholar 

  11. West MA, Hackam DJ, Baker J, Rodriguez JL, Bellingham J, Rotstein OD (1997) Mechanism of decreased in vitro murine macrophage cytokine release after exposure to carbon dioxide. Am Surg 226:179–190

    CAS  Google Scholar 

  12. Steeg PS, Bevilacqua G, Kopper L, Thorgeirsson UP, Talmadge JE, Liotta LA, Sobel ME (1988) Evidence for a novel gene associated with low tumor metastatic potential. J Natl Cancer Inst 80:200–204

    Article  CAS  PubMed  Google Scholar 

  13. Barnes R, Masood S, Barker E et al (1991) Low nm23 protein expression in infiltrating ductal breast carcinomas correlates with reduced patient survival. Am J Pathol 139:245–250

    CAS  PubMed Central  PubMed  Google Scholar 

  14. Ayhan A, Yasui W, Yokozaki H, Kitadai Y, Tahara E (1993) Reduced expression of nm23 protein is associated with advanced tumor stage and distant metastases in human colorectal carcinomas. Virchows Arch B cell Pathol Incl Mol Pathol 63:213–218

    Article  CAS  PubMed  Google Scholar 

  15. Passlick B, Sienel W, Seen-Hibler R, Wöckel W, Thetter O, Mutschler W, Pantel K (2000) Overexpression of matrix metalloproteinase 2 predicts unfavorable outcome in early-stage non-small cell lung cancer. Clin Cancer Res 6:3944–3948

    CAS  PubMed  Google Scholar 

  16. Tryggvason K, Hoyhtya M, Pyke C (1993) Type IV collagenases in invasive tumors. Breast Cancer Res Treat 24:209–218

    Article  CAS  PubMed  Google Scholar 

  17. Nomura H, Sato H, Seiki M, Mai M, Okada Y (1995) Expression of membrane-type matrix metalloproteinase in human gastric carcinomas. Cancer Res 55:3263–3266

    CAS  PubMed  Google Scholar 

  18. Wu ZY, Li JH, Zhan WH, He YL (2006) Lymph node micrometastasis and its correlation with MMP-2 expression in gastric carcinoma. World J Gastroenterol 12:2941–2944

    CAS  PubMed Central  PubMed  Google Scholar 

  19. Sammour T, Kahokehr A, Hill A (2008) Meta-analysis of the effect of warm humidified insufflation on pain after laparoscopy. Br J Surg 95:950–956

    Article  CAS  PubMed  Google Scholar 

  20. Binda M, Molinas C, Hansen P, Koninckx P (2006) Effect of desiccation and temperature during laparoscopy on adhesion formation in mice. Fertil Stertil 86:166–175

    Article  Google Scholar 

  21. Ott DE (2001) Laparoscopy and tribology: the effect of laparoscopic gas on peritoneal fluid. J Am Assoc Gynecolo Laparosc 8:117–123

    Article  CAS  Google Scholar 

  22. Volz J, Köster S, Spacek Z, Paweletz N (1999) Characteristic alterations of the peritoneum after carbon dioxide pneumoperitoneum. Surg Endosc 13:611–614

    Article  CAS  PubMed  Google Scholar 

  23. Hao YX, Zhong H, Yu PW, Zhang C, Zeng DZ, Shi Y, Tang B (2009) Effects of HIF-1alpha on human gastric cancer cell apoptosis at different CO2 pressures. Clin Exp Med 9:139–147

    Article  CAS  PubMed  Google Scholar 

  24. Hendriksen EM, Span PN, Schuuring J, Peters JP, Sweep FC, van der Kogel AJ, Bussink J (2009) Angiogenesis, hypoxia and VEGF expression during tumour growth in a human xenograft tumour model. Microvasc Res 77:96–103

    Article  CAS  PubMed  Google Scholar 

  25. Crowther M, Brown N, Bishop E, Lewis C (2001) Microenvironmental influence on macrophage regulation of angiogenesis in wounds and malignant tumours. J Leukoc Biol 70:478–490

    CAS  PubMed  Google Scholar 

  26. Gao QL, Ma D, Meng L, Wang SX, Wang CY, Lu YP, Zhang AL, Li J (2004) Association between Nm23-H1 gene expression and metastasis of ovarian carcinoma. Ai Zheng 23:650–654

    CAS  PubMed  Google Scholar 

  27. Galani E, Sgouros J, Petropoulou C, Janinis J, Aravantinos G, Dionysiou-Asteriou D, Skarlos D, Gonos E (2002) Correlation of MDR-1, nm23-H1 and H Sema E gene expression with histopathological findings and clinical outcome in ovarian and breast cancer patients. Anticancer Res 22:2275–2280

    CAS  PubMed  Google Scholar 

  28. Kapitanovic S, Spaventi R, Vujsic S, Petrovic Z, Kurjak A, Pavelic ZP, Gluckman JL, Stambrook PJ, Pavelic K (1995) nm23-H1 gene expression in ovarian tumors—a potential tumor marker. Anticancer Res 15:587–590

    CAS  PubMed  Google Scholar 

  29. Lee E, Jeong J, Kim SE, Song EJ, Kang SW, Lee KJ (2009) Multiple functions of Nm23-H1 are regulated by oxido-reduction system. PLoS One 4:e7949

    Article  PubMed Central  PubMed  Google Scholar 

  30. Denkert C, Siegert A, Leclere A, Turzynski A, Hauptmann S (2002) An inhibitor of stress-activated MAP-kinases reduces invasion and MMP-2 expression of malignant melanoma cells. Clin Exp Metastasis 19:79–85

    Article  CAS  PubMed  Google Scholar 

  31. Kubben FJ, Sier CF, van Duijn W, Griffioen G, Hanemaaijer R, van de Velde CJ, van Krieken JH, Lamers CB, Verspaget HW (2006) Matrix metalloproteinase-2 is a consistent prognostic factor in gastric cancer. Br J Cancer 94:1035–1040

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Ridgway PF, Smith A, Ziprin P, Jones TL, Paraskeva PA, Peck DH, Darzi AW (2002) Pneumoperitoneum augmented tumor invasiveness is abolished by matrix metalloproteinase blockade. Surg Endosc 16:533–536

    Article  CAS  PubMed  Google Scholar 

  33. Che G, Chen J, Liu L, Wang Y, Li L, Qin Y, Zhou Q (2006) Transfection of nm23-H1 increased expression of beta-Catenin, E-Cadherin and TIMP-1 and decreased the expression of MMP-2, CD44v6 and VEGF and inhibited the metastatic potential of human non-small cell lung cancer cell line L9981. Neoplasma 53:530–537

    CAS  PubMed  Google Scholar 

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Conflict of interest

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Authors and Affiliations

  1. Department of Obstetrics and Gynecology, The First Affiliated Hospital of Jinan University, Guangzhou, 510630, China

    Ying Zhang & Xin Luo

  2. Department of Obstetrics and Gynecology, The Affiliated Hospital of Guangdong Medical College, Zhanjiang, 524001, China

    Ying Zhang, Bingjuan Fan, Huijuan Chen, Aizhen Fu & Jinzhi Huang

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  1. Ying Zhang
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  2. Xin Luo
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  3. Bingjuan Fan
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Correspondence to Xin Luo.

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Zhang, Y., Luo, X., Fan, B. et al. Effect of CO2 pneumoperitoneum on the proliferation of human ovarian cancer cell line SKOV-3 and the expression of NM23-H1 and MMP-2. Arch Gynecol Obstet 291, 403–411 (2015). https://doi.org/10.1007/s00404-014-3414-2

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  • DOI: https://doi.org/10.1007/s00404-014-3414-2

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