Modified Adenovirus Reduces De Novo Peritoneal Adhesions in Rats and Limits Off-Target Transfection. Role of EZH2 in Adhesion Formation

REFERENCES

• Mavros MN, Velmahos GC, Lee J, Larentzakis A, Kaafarani HM. Morbidity related to concomitant adhesions in abdominal surgery. J Surg Res. 2014;192:286–292.
   PubMed Web of Science ®Google Scholar
• ten Broek RP, Stommel MW, Strik C, van Laarhoven CJ, Keus F, van Goor H. Benefits and harms of adhesion barriers for abdominal surgery: a systematic review and meta-analysis. Lancet. 2014;383:48–59.
   PubMed Web of Science ®Google Scholar
• Sikirica V, Bapat B, Candrilli SD, Davis KL, Wilson M, Johns A. The inpatient burden of abdominal and gynecological adhesiolysis in the US. BMC Surg. 2011;11:13.
   PubMed Web of Science ®Google Scholar
• Ellis H, Crowe A. Medico-legal consequences of post-operative intra-abdominal adhesions. Int J Surg. 2009;7:187–191.
   PubMed Web of Science ®Google Scholar
• Atta HM. Prevention of peritoneal adhesions: a promising role for gene therapy. World J Gastroenterol. 2011;17:5049–5058.
   PubMed Web of Science ®Google Scholar
• Rodgers KE, Girgis W, St Amand K, Campeau JD, diZerega GS. Reduction of adhesion formation by intraperitoneal administration of various anti-inflammatory agents. J Invest Surg. 1998;11:327–339.
   PubMed Web of Science ®Google Scholar
• Holmdahl L, Eriksson E, al-Jabreen M, Risberg B. Fibrinolysis in human peritoneum during operation. Surgery. 1996;119:701–705.
   PubMed Web of Science ®Google Scholar
• Holmdahl L, Falkenberg M, Ivarsson ML, Risberg B. Plasminogen activators and inhibitors in peritoneal tissue. APMIS. 1997;105:25–30.
   PubMed Web of Science ®Google Scholar
• Scott-Coombes D, Whawell S, Vipond MN, Thompson J. Human intraperitoneal fibrinolytic response to elective surgery. Br J Surg. 1995;82:414–417.
   PubMed Web of Science ®Google Scholar
• Brokelman WJ, Holmdahl L, Janssen IM, Falk P, Bergstrom M, Klinkenbijl JH, et al. Decreased peritoneal tissue plasminogen activator during prolonged laparoscopic surgery. J Sur Res. 2009;151:89–93.
   PubMed Web of Science ®Google Scholar
• Arung W, Jehaes F, Cheramy JP, Defraigne JO, Meurisse M, Honoré P, Drion P, Detry O. Effects of parecoxib on the prevention of postoperative peritoneal adhesions in rats. J Invest Surg. 2013;26:340–346.
   PubMed Web of Science ®Google Scholar
• Sulaiman H, Dawson L, Laurent GJ, Bellingan GJ, Herrick SE. Role of plasminogen activators in peritoneal adhesion formation. Biochem Soc Trans. 2002;30:126–131.
   PubMed Web of Science ®Google Scholar
• Hellebrekers BW, Trimbos-Kemper TC, Boesten L, Jansen FW, Kolkman W, Trimbos JB, et al. Preoperative predictors of postsurgical adhesion formation and the prevention of adhesions with plasminogen activator (PAPA-study): results of a clinical pilot study. Fertil Steril. 2009;91:1204–1214.
   PubMed Web of Science ®Google Scholar
• Atta HM, Al-Hendy A, El-Rehany MA, Dewerchin M, Abdel Raheim SR, Abdel Ghany H, et al. Adenovirus-mediated overexpression of human tissue plasminogen activator prevents peritoneal adhesion formation/reformation in rats. Surgery. 2009;146:12–17.
   PubMed Web of Science ®Google Scholar
• Buckenmaier CC, 3rd, Summers MA, Hetz SP. Effect of the antiadhesive treatments, carboxymethylcellulose combined with recombinant tissue plasminogen activator and seprafilm, on bowel anastomosis in the rat. Am Surg. 2000;66:1041–1045.
   PubMed Web of Science ®Google Scholar
• Hellebrekers BW, Trimbos-Kemper TC, Trimbos JB, Emeis JJ, Kooistra T. Use of fibrinolytic agents in the prevention of postoperative adhesion formation. Fertil Steril 2000;74:203–212.
   PubMed Web of Science ®Google Scholar
• Atta H, El-Rehany M, Roeb E, Abdel-Ghany H, Ramzy M, Gaber S. Mutant matrix metalloproteinase-9 reduces postoperative peritoneal adhesions in rats. Int J Surg. 2016;26:58–63.
   PubMed Web of Science ®Google Scholar
• Nair S, Saed GM, Atta HM, Rajaratnam V, Diamond MP, Curiel DT, et al. Towards gene therapy of postoperative adhesions: fiber and transcriptional modifications enhance adenovirus targeting towards human adhesion cells. Gynecol Obstet Invest. 2013;76:119–124.
   PubMed Web of Science ®Google Scholar
• Tsuruta Y, Pereboeva L, Glasgow JN, Luongo CL, Komarova S, Kawakami Y, et al. Reovirus sigma1 fiber incorporated into adenovirus serotype 5 enhances infectivity via a CAR-independent pathway. Biochem Biophys Res Commun. 2005;335:205–214.
   PubMed Web of Science ®Google Scholar
• Mercier GT, Campbell JA, Chappell JD, Stehle T, Dermody TS, Barry MA. A chimeric adenovirus vector encoding reovirus attachment protein sigma1 targets cells expressing junctional adhesion molecule 1. Proc Natl Acad Sci U S A. 2004;101:6188–6193.
   PubMed Web of Science ®Google Scholar
• Tsuruta Y, Pereboeva L, Breidenbach M, Rein DT, Wang M, Alvarez RD, et al. A fiber-modified mesothelin promoter-based conditionally replicating adenovirus for treatment of ovarian cancer. Clin Cancer Res. 2008;14:3582–3588.
   PubMed Web of Science ®Google Scholar
• Shaw T, Martin P. Epigenetic reprogramming during wound healing: loss of polycomb-mediated silencing may enable upregulation of repair genes. EMBO Rep. 2009;10:881–886.
   PubMed Web of Science ®Google Scholar
• Cao R, Zhang Y. The functions of E(Z)/EZH2-mediated methylation of lysine 27 in histone H3. Curr Opin Genet Dev. 2004;14:155–164.
   PubMed Web of Science ®Google Scholar
• Vire E, Brenner C, Deplus R, Blanchon L, Fraga M, Didelot C, et al. The polycomb group protein EZH2 directly controls DNA methylation. Nature. 2006;439:871–874.
   PubMed Web of Science ®Google Scholar
• Grow DR, Coddington CC, Hsiu JG, Mikich Y, Hodgen GD. Role of hypoestrogenism or sex steroid antagonism in adhesion formation after myometrial surgery in primates. Fertil Steril. 1996;66:140–147.
   PubMed Web of Science ®Google Scholar
• Reeves MB. Chromatin-mediated regulation of cytomegalovirus gene expression. Virus Res. 2011;157:134–143.
   PubMed Web of Science ®Google Scholar
• Wallwiener D, Meyer A, Bastert G. Adhesion formation of the parietal and visceral peritoneum: an explanation for the controversy on the use of autologous and alloplastic barriers?. Fertil Steril. 1998;69:132–137.
   PubMed Web of Science ®Google Scholar
• Holmdahl L, Eriksson E, Eriksson BI, Risberg B. Depression of peritoneal fibrinolysis during operation is a local response to trauma. Surgery. 1998;123:539–544.
   PubMed Web of Science ®Google Scholar
• Peterson GL. Determination of total protein. Methods Enzymol. 1983;91:95–119.
   PubMed Web of Science ®Google Scholar
• Kiernan JA. Indigogenic substrates for detection and localization of enzymes. Biotech Histochem. 2007;82:73–103.
   PubMed Web of Science ®Google Scholar
• Atta HM, Al-Hendy A, Salama SA, Shaker OG, Hammam OA. Low-dose simultaneous delivery of adenovirus encoding hepatocyte growth factor and vascular endothelial growth factor in dogs enhances liver proliferation without systemic growth factor elevation. Liver Int. 2009;29:1022–1030.
   PubMed Web of Science ®Google Scholar
• Atta H, El-Rehany M, Hammam O, Abdel-Ghany H, Ramzy M, Roderfeld M, et al. Mutant MMP-9 and HGF gene transfer enhance resolution of CCl4-induced liver fibrosis in rats: role of ASH1 and EZH2 methyltransferases repression. PloS One. 2014;9:e112384.
   PubMed Web of Science ®Google Scholar
• Tao N, Gao GP, Parr M, Johnston J, Baradet T, Wilson JM, et al. Sequestration of adenoviral vector by Kupffer cells leads to a nonlinear dose response of transduction in liver. MolTher. 2001;3:28–35.
   Google Scholar
• Hobson KG, DeWing M, Ho HS, Wolfe BM, Cho K, Greenhalgh DG. Expression of transforming growth factor beta1 in patients with and without previous abdominal surgery. Arch Surg. 2003;138:1249–1252.
   PubMedGoogle Scholar
• Falk P, Angenete E, Bergström M, Ivarsson ML. TGF-β1 promotes transition of mesothelial cells into fibroblast phenotype in response to peritoneal injury in a cell culture model. Int J Surg. 2013;11:977–982.
   PubMed Web of Science ®Google Scholar
• Gorvy DA, Herrick SE, Shah M, Ferguson MW. Experimental manipulation of transforming growth factor-beta isoforms significantly affects adhesion formation in a murine surgical model. Am J Pathol. 2005;167:1005–1019.
   PubMed Web of Science ®Google Scholar
• Jin X, Ren S, Macarak E, Rosenbloom. Pathobiological mechanisms of peritoneal adhesions: The mesenchymal transition of rat peritoneal mesothelial cells induced by TGF-β1 and IL-6 requires activation of Erk1/2 and Smad2 linker region phosphorylation. Matrix Biol. 2016 (in press);51:55–64. http://dx.doi.org/10.1016/j.matbio.2016.01.017
   PubMed Web of Science ®Google Scholar
• Zhang H, Song Y, Li Z, Zhang T, Zeng L. Evaluation of breviscapine on prevention of experimentally induced abdominal adhesions in rats. Am J Surg. 2015 (in press);211:1143–1152. doi: 10.1016/j.amjsurg.2015.05.037.
   Web of Science ®Google Scholar
• Guo H, Leung JC, Cheung JS, Chan LY, Wu EX, Lai KN. Non-viral Smad7 gene delivery and attenuation of postoperative peritoneal adhesion in an experimental model. Br J Surg. 2009;96:1323–1335.
   PubMed Web of Science ®Google Scholar
• Khare R, Hillestad ML, Xu Z, Byrnes AP, Barry MA. Circulating antibodies and macrophages as modulators of adenovirus pharmacology. J Virol. 2013;87:3678–3686.
   PubMed Web of Science ®Google Scholar
• Xu Z, Tian J, Smith JS, Byrnes AP. Clearance of adenovirus by Kupffer cells is mediated by scavenger receptors, natural antibodies, and complement. J Virol. 2008;82:11705–11713.
   PubMed Web of Science ®Google Scholar
• Zhou ZH, Tzioufas AG, Notkins AL. Properties and function of polyreactive antibodies and polyreactive antigen-binding B cells. J Autoimmun. 2007;29:219–228.
   PubMed Web of Science ®Google Scholar
• Ellis J, Yao S. Retrovirus silencing and vector design: relevance to normal and cancer stem cells?. Curr Gene Ther. 2005;5:367–373.
   PubMed Web of Science ®Google Scholar
• Minarovits J. Microbe-induced epigenetic alterations in host cells: the coming era of patho-epigenetics of microbial infections. A review. Acta Microbiol Immunol Hung. 2009;56:1–19.
   PubMed Web of Science ®Google Scholar
• Mann J, Chu DC, Maxwell A, Oakley F, Zhu NL, Tsukamoto H, et al. MeCP2 controls an epigenetic pathway that promotes myofibroblast transdifferentiation and fibrosis. Gastroenterol. 2010;138:705–14.
   PubMed Web of Science ®Google Scholar
• Yang MD, Chiang YM, Higashiyama R, Asahina K, Mann DA, Mann J, et al. Rosmarinic acid and baicalin epigenetically derepress peroxisomal proliferator-activated receptor gamma in hepatic stellate cells for their antifibrotic effect. Hepatol. 2012;55:1271–1281.
   PubMed Web of Science ®Google Scholar
• Coward WR, Feghali-Bostwick CA, Jenkins G, Knox AJ, Pang L. A central role for G9a and EZH2 in the epigenetic silencing of cyclooxygenase-2 in idiopathic pulmonary fibrosis. FASEB J. 2014;28:3183–3196.
   PubMed Web of Science ®Google Scholar
• Cassidy MR, Sheldon HK, Gainsbury ML, Gillespie E, Kosaka H, Heydrick S, et al. The neurokinin 1 receptor regulates peritoneal fibrinolytic activity and postoperative adhesion formation. J Surg Res. 2014;191:12–18.
   PubMed Web of Science ®Google Scholar