Preventing postoperative metastatic disease by inhibiting surgery-induced dysfunction in natural killer cells

Cancer Research

Volumn 73, Issue 1, 2013, Pages 97-107

  Tai, Lee Hwa ^a   De Souza, Christiano Tanese ^a   Bélanger, Simon ^b   Ly, Lundi ^a,b   Alkayyal, Almohanad A ^a,b   Zhang, Jiqing ^a   Rintoul, Julia L ^a,b   Ananth, Abhirami A ^a,b   Lam, Tiffany ^a   Breitbach, Caroline J ^c   Falls, Theresa J ^a   Kirn, David H ^c   Bell, John C ^a,b,c   Makrigiannis, Andrew P ^b   Auer, Rebecca A ^a,b  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

^c Jennerex Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PEXASTIMOGENE DEVACIREPVEC; VIRUS VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CANCER RECURRENCE; CANCER SURVIVAL; CELL ACTIVITY; CELL COUNT; CELL FUNCTION; CELL MIGRATION; CELL POPULATION; CONTROLLED STUDY; CORRELATION ANALYSIS; DRUG EFFICACY; HUMAN; HUMAN CELL; IN VIVO STUDY; LUNG METASTASIS; MOUSE; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; NONHUMAN; POSTOPERATIVE COMPLICATION; POXVIRUS; PRIORITY JOURNAL; SPLEEN; SURGICAL STRESS; TREATMENT OUTCOME;

ANIMALS; FLOW CYTOMETRY; HUMANS; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NEOPLASM METASTASIS; NEOPLASMS, EXPERIMENTAL; NEOPLASTIC CELLS, CIRCULATING; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; STRESS, PHYSIOLOGICAL; SURGICAL PROCEDURES, OPERATIVE;

EID: 84871959360     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-1993     Document Type: Article

References (47)

1. Tyzzer EE. Factors in the production and growth of tumor metastases. J Med Res 1913;28:309-32, 301.
2. Tsuchiya Y, Sawada S, Yoshioka I, Ohashi Y, Matsuo M, Harimaya Y, et al. Increased surgical stress promotes tumor metastasis. Surgery 2003;133:547-55.
3. Glasner A, Avraham R, Rosenne E, Benish M, Zmora O, Shemer S, et al. Improving survival rates in two models of spontaneous postoperative metastasis in mice by combined administration of a beta-adrenergic antagonist and a cyclooxygenase-2 inhibitor. J Immunol 2010;184:2449-57.
4. Lerut T, Moons J, Coosemans W, Van Raemdonck D, De Leyn P, Decaluwe H, et al. Postoperative complications after transthoracic esophagectomy for cancer of the esophagus and gastroesophageal junction are correlated with early cancer recurrence: role of systematic grading of complications using the modified clavien classification. Ann Surg 2009;250:798-807.
5. Eberhardt JM, Kiran RP, Lavery IC. The impact of anastomotic leak and intra-abdominal abscess on cancer-related outcomes after resection for colorectal cancer: a case control study. Dis Colon Rectum 2009;52:380-6.
6. Fortner JG. Inadvertent spread of cancer at surgery. J Surg Oncol 1993;53:191-6.
7. Yamaguchi K, Takagi Y, Aoki S, Futamura M, Saji S. Significant detection of circulating cancer cells in the blood by reverse transcriptase-polymerase chain reaction during colorectal cancer resection. Ann Surg 2000;232:58-65.
8. Belizon A, Balik E, Feingold DL, Bessler M, Arnell TD, Forde KA, et al. Major abdominal surgery increases plasma levels of vascular endothelial growth factor: open more so than minimally invasive methods. Ann Surg 2006;244:792-8.
9. Pera M, Nelson H, Rajkumar SV, Young-Fadok TM, Burgart LJ. Influence of postoperative acute-phase response on angiogenesis and tumor growth: open vs. laparoscopic-assisted surgery in mice. J Gastrointest Surg 2003;7:783-90.
10. Paterlini-Brechot P, Benali NL. Circulating tumor cells (CTC) detection: clinical impact and future directions. Cancer Lett 2007;253:180-204.
11. Karl A, Tritschler S, Hofmann S, Stief CG, Schindlbeck C. Perioperative search for circulating tumor cells in patients undergoing radical cystectomy for bladder cancer. Eur J Med Res 2009;14:487-90.
12. Coffey JC, Wang JH, Smith MJ, Bouchier-Hayes D, Cotter TG, Redmond HP. Excisional surgery for cancer cure: therapy at a cost. Lancet Oncol 2003;4:760-8.
13. Espi A, Arenas J, Garcia-Granero E, Marti E, Lledo S. Relationship of curative surgery on natural killer cell activity in colorectal cancer. Dis Colon Rectum 1996;39:429-34.
14. Pollock RE, Lotzova E, Stanford SD. Mechanism of surgical stress impairment of human perioperative natural killer cell cytotoxicity. Arch Surg 1991;126:338-42.
15. Pollock RE, Lotzova E, Stanford SD. Surgical stress impairs natural killer cell programming of tumor for lysis in patients with sarcomas and other solid tumors. Cancer 1992;70:2192-202.
16. Page GG, Blakely WP, Ben-Eliyahu S. Evidence that postoperative pain is a mediator of the tumor-promoting effects of surgery in rats. Pain 2001;90:191-9.
17. Ben-Eliyahu S, Page GG, Yirmiya R, Shakhar G. Evidence that stress and surgical interventions promote tumor development by suppressing natural killer cell activity. Int J Cancer 1999;80:880-8.
18. Benish M, Bartal I, Goldfarb Y, Levi B, Avraham R, Raz A, et al. Perioperative use of beta-blockers and COX-2 inhibitors may improve immune competence and reduce the risk of tumor metastasis. Ann Surg Oncol 2008;15:2042-52.
19. Goldfarb Y, Sorski L, Benish M, Levi B, Melamed R, Ben-Eliyahu S. Improving postoperative immune status and resistance to cancer metastasis: a combined perioperative approach of immunostimulation and prevention of excessive surgical stress responses. Ann Surg 2011;253:798-810.
20. Tartter PI, Steinberg B, Barron DM, Martinelli G. The prognostic significance of natural killer cytotoxicity in patients with colorectal cancer. Arch Surg 1987;122:1264-8.
21. Fujisawa T, Yamaguchi Y. Autologous tumor killing activity as a prognostic factor in primary resected nonsmall cell carcinoma of the lung. Cancer 1997;79:474-81.
22. Guillot B, Bessis D, Dereure O. Mucocutaneous side effects of antineoplastic chemotherapy. Expert Opin Drug Saf 2004;3:579-87.
23. Klatte T, Ittenson A, Rohl FW, Ecke M, Allhoff EP, Bohm M. Perioperative immunomodulation with interleukin-2 in patients with renal cell carcinoma: results of a controlled phase II trial. Br J Cancer 2006;95:1167-73.
24. Oosterling SJ, van der Bij GJ, Mels AK, Beelen RH, Meijer S, van Egmond M, et al. Perioperative IFN-alpha to avoid surgically induced immune suppression in colorectal cancer patients. Histol Histopathol 2006;21:753-60.
25. Deehan DJ, Heys SD, Ashby J, Eremin O. Interleukin-2 (IL-2) augments host cellular immune reactivity in the perioperative period in patients with malignant disease. Eur J Surg Oncol 1995;21:16-22.
26. Houvenaeghel G, Bladou F, Blache JL, Olive D, Monges G, Jacquemier J, et al. Tolerance and feasibility of perioperative treatment with interferon-alpha 2a in advanced cancers. Int Surg 1997;82:165-9.
27. Breitbach CJ, Burke J, Jonker D, Stephenson J, Haas AR, Chow LQ, et al. Intravenous delivery of a multi-mechanistic cancer-targeted oncolytic poxvirus in humans. Nature 2011;477:99-102.
28. Kirn DH, Thorne SH. Targeted and armed oncolytic poxviruses: a novel multi-mechanistic therapeutic class for cancer. Nat Rev Cancer 2009;9:64-71.
29. Rintoul JL, Lemay CG, Tai LH, Stanford MM, Falls TJ, de Souza CT, et al. ORFV: a novel oncolytic and immune stimulating parapoxvirus therapeutic. Mol Ther 2012;20:1148-57.
30. Kirstein JM, Graham KC, Mackenzie LT, Johnston DE, Martin LJ, Tuck AB, et al. Effect of anti-fibrinolytic therapy on experimental melanoma metastasis. Clin Exp Metastasis 2009;26:121-31.
31. Savory LJ, Stacker SA, Fleming SB, Niven BE, Mercer AA. Viral vascular endothelial growth factor plays a critical role in orf virus infection. J Virol 2000;74:10699-706.
32. Le Boeuf F, Diallo JS, McCart JA, Thorne S, Falls T, Stanford M, et al. Synergistic interaction between oncolytic viruses augments tumor killing. Mol Ther 2010;18:888-95.
33. Patel R, Belanger S, Tai LH, Troke AD, Makrigiannis AP. Effect of Ly49 haplotype variance on NK cell function and education. J Immunol 2010;185:4783-92.
34. Seth R, Tai LH, Falls T, de Souza CT, Bell JC, Carrier M, et al. Surgical stress promotes the development of cancer metastases by a coagulation-dependent mechanism involving Natural Killer cells in a murine model. Ann Surg. Epub 2012 Oct 26. PMID: 23108132.
35. Gorelik E, Wiltrout RH, Okumura K, Habu S, Herberman RB. Role of NK cells in the control of metastatic spread and growth of tumor cells in mice. Int J Cancer 1982;30:107-12.
36. Hanna N. The role of natural killer cells in the control of tumor growth and metastasis. Biochim Biophys Acta 1985;780:213-26.
37. Champsaur M, Lanier LL. Effect of NKG2D ligand expression on host immune responses. Immunol Rev 2010;235:267-85.
38. Dong Z, Cruz-Munoz ME, Zhong MC, Chen R, Latour S, Veillette A. Essential function for SAP family adaptors in the surveillance of hematopoietic cells by natural killer cells. Nat Immunol 2009;10:973-80.
39. Shakhar G, Ben-Eliyahu S. Potential prophylactic measures against postoperative immunosuppression: could they reduce recurrence rates in oncological patients? Ann Surg Oncol 2003;10:972-92.
40. Frey AB. Myeloid suppressor cells regulate the adaptive immune response to cancer. J Clin Invest 2006;116:2587-90.
41. + regulatory T cells for immunologic self-tolerance and negative control of immune responses. Annu Rev Immunol 2004;22:531-62.
42. + regulatory T cells inhibit natural killer cell functions in a transforming growth factor-beta-dependent manner. J Exp Med 2005;202:1075-85.
43. Nichols PH, Ramsden CW, Ward U, Sedman PC, Primrose JN. Perioperative immunotherapy with recombinant interleukin 2 in patients undergoing surgery for colorectal cancer. Cancer Res 1992;52:5765-9.
44. Nichols PH, Ramsden CW, Ward U, Trejdosiewicz LK, Ambrose NS, Primrose JN. Peri-operative modulation of cellular immunity in patients with colorectal cancer. Clin Exp Immunol 1993;94:4-10.
45. Sedman PC, Ramsden CW, Brennan TG, Giles GR, Guillou PJ. Effects of low dose perioperative interferon on the surgically induced suppression of antitumour immune responses. Br J Surg 1988;75:976-81.
46. Romano F, Cesana G, Berselli M, Gaia Piacentini M, Caprotti R, Bovo G, et al. Biological, histological, and clinical impact of preoperative IL-2 administration in radically operable gastric cancer patients. J Surg Oncol 2004;88:240-7.
47. Elias D, Farace F, Triebel F, Hattchouel JM, Pignon JP, Lecesne A, et al. Phase I-II randomized study on prehepatectomy recombinant interleukin-2 immunotherapy in patients with metastatic carcinoma of the colon and rectum. J Am Coll Surg 1995;181:303-10.