Journal of Surgical Research
Volume 139, Issue 1 , Pages 36-44 , 1 May 2007

Impaired Natural Killer Cell Lysis in Breast Cancer Patients with High Levels of Psychological Stress is Associated with Altered Expression of Killer Immunoglobin-Like Receptors

  • Kimberly A. Varker, M.D.

      Affiliations

    • Comprehensive Cancer Center, The Ohio State University, Columbus, Ohio
  • ,
  • Catherine E. Terrell, B.S.

      Affiliations

    • Comprehensive Cancer Center, The Ohio State University, Columbus, Ohio
    • Department of Psychology, The Ohio State University, Columbus, Ohio
  • ,
  • Marilyn Welt, B.S.

      Affiliations

    • Comprehensive Cancer Center, The Ohio State University, Columbus, Ohio
    • Department of Psychology, The Ohio State University, Columbus, Ohio
  • ,
  • Samer Suleiman, B.S.

      Affiliations

    • Comprehensive Cancer Center, The Ohio State University, Columbus, Ohio
    • Department of Psychology, The Ohio State University, Columbus, Ohio
  • ,
  • Lisa Thornton, Ph.D.

      Affiliations

    • Department of Psychology, The Ohio State University, Columbus, Ohio
  • ,
  • Barbara L. Andersen, Ph.D.

      Affiliations

    • Comprehensive Cancer Center, The Ohio State University, Columbus, Ohio
    • Department of Psychology, The Ohio State University, Columbus, Ohio
    • Institute of Behavioral Medical Research, The Ohio State University, Columbus, Ohio
  • ,
  • William E. Carson III, M.D.

      Affiliations

    • Comprehensive Cancer Center, The Ohio State University, Columbus, Ohio
    • College of Medicine, The Ohio State University, Columbus, Ohio
    • Department of Surgery, The Ohio State University, Columbus, Ohio
    • Corresponding Author InformationTo whom correspondence and reprint requests should be addressed at Division of Surgical Oncology, The Ohio State University, N924 Doan Hall, 410 W. 10th Avenue, Columbus, OH 43210.

Received 18 April 2006

References 

  1. Carlson LE, Angen M, Cullum J, et al. High levels of untreated distress and fatigue in cancer patients. Br J Cancer. 2004;90:2297
  2. Andersen BL, Kiecolt-Glaser JK, Glaser R. A biobehavioral model of cancer stress and disease course. Am Psychol. 1994;49:389
  3. Andersen BL. Biobehavioral outcomes following psychological interventions for cancer patients. J Consult Clin Psychol. 2003;70:590;Erratum in J Consult Clin Psychol 2003;71:481.
  4. Herschbach P, Keller M, Knight L, et al. Psychological problems of cancer patients: A cancer distress screening with a cancer-specific questionnaire. Br J Cancer. 2004;91:504
  5. Iwamitsu Y, Shimoda K, Abe H, et al. Differences in emotional distress between breast tumor patients with emotional inhibition and those with emotional expression. Psychiatry Clin Neurosci. 2003;57:289
  6. Montgomery GH, David D, Goldfarb AB, et al. Sources of anticipatory distress among breast surgery patients. J Behav Med. 2003;26:153
  7. Morasso G, Costantini M, Baracco G, et al. Assessing psychological distress in cancer patients: Validation of a self-administered questionnaire. Oncology. 1996;53:295
  8. Sundin EC, Horowitz MJ. Horowitz’s impact of event scale: Evaluation of 20 years of use. Psychosom Med. 2003;65:870
  9. van’t Spijker A, Trijsburg RW, Duivenvoorden HJ. Psychological sequelae of cancer diagnosis: A meta-analytical review of 58 studies after 1980. Psychosom Med. 1997;59:280
  10. Goodwin PJ, Ennis M, Bordeleau LJ, et al. Health-related quality of life and psychosocial status in breast cancer prognosis: Analysis of multiple variables. J Clin Oncol. 2004;22:4184
  11. Thomas BC, Mohan VN, Thomas I, et al. Development of a distress inventory for cancer: Preliminary results. J Postgrad Med. 2002;48:16
  12. Weiss DS, Horowitz MJ, Wilner N. The stress response rating scale: A clinician’s measure for rating the response to serious life events. Br J Clin Psychol. 1984;23:202
  13. Horowitz M, Wilner N, William A. Impact of event scale: A measure of subjective stress. Psychosom Med. 1979;41:209
  14. Sundin EC, Horowitz MJ. Impact of event scale: Psychometric properties. Br J Psychiatry. 2002;180:205
  15. Andersen BL, Farrar WB, Golden-Kreutz D, et al. Stress and immune responses after surgical treatment for regional breast cancer. J Natl Cancer Inst. 1998;90:30
  16. Andersen BL, Farrar WB, Golden-Kreutz DM, et al. Psychological, behavioral, and immune changes after a psychological intervention: A clinical trial. J Clin Oncol. 2004;22:3570
  17. McGregor BA, Antoni MH, Boyers A, et al. Cognitive-behavioral stress management increases benefit finding and immune function among women with early-stage breast cancer. J Psychosom Res. 2004;56:1
  18. Bonilla F, Alvarez-Mon M, Merino F, et al. Natural killer activity in patients with breast cancer. Eur J Gynaecol Oncol. 1990;11:103
  19. Esterling BA, Keicolt-Glaser JK, Bodnar JC, et al. Chronic stress, social support, and persistent alterations in the natural killer cell response to cytokines in older adults. Health Psychol. 1994;13:291
  20. Esterling BA, Kiecolt-Glaser JK, Glaser R. Psychosocial modulation of cytokine-induced natural killer cell activity in older adults. Psychosom Med. 1996;58:264–272
  21. Garner WL, Minton JP, James AG, et al. Human breast cancer and impaired NK cell function. J Surg Oncol. 1983;24:64
  22. Hebert TB, Cohen S. Depression and immunity: A meta-analytic review. Psychol Bull. 1993;113:472
  23. Kiecolt-Glaser JK, Marucha WB, Mercado AM, et al. Slowing of wound healing by psychological stress. Lancet. 1995;346:1194
  24. Schedlowski M, Jacobs R, Stratmann G, et al. Changes in natural killer cells during acute psychological stress. J Clin Immunol. 1993;13:119
  25. Uchida A, Kolb R, Micksche M. Generation of suppressor cells for natural killer activity in cancer patients after surgery. J Natl Cancer Inst. 1982;68:735
  26. Beitsch P, Lotzova E, Hortobagyi G, et al. Natural immunity in breast cancer patients during neoadjuvant chemotherapy and after surgery. Surg Oncol. 1994;3:211
  27. McCulloch PG, MacIntryre A. Effects of surgery on the generation of lymphokine-activated killer cells in patients with breast cancer. Br J Surg. 1993;80:1005
  28. Pollock RE, Lotzova E, Stanford SD. Mechanism of surgical stress impairment of human perioperative natural killer cell cytotoxicity. Arch Surg. 1991;126:338
  29. 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
  30. Farag SS, Caligiuri MA. Human natural killer cell development and biology. Blood Rev. 2006;20:123
  31. Carson WE, Shapiro CL, Crespin TR, et al. Cellular immunity in breast cancer patients completing taxane treatment. Clin Cancer Res. 2004;10:3401
  32. Snyder MR, Weyand CM, Goronzy JJ. The double life of NK receptors: stimulation or co-stimulation?. Trends Immunol. 2004;25:25
  33. Segerstrom SC, Miller GE. Psychological stress and the human immune system: A meta-analytic study of 30 years of inquiry. Psychol Bull. 2004;130:601
  34. Light KC, Girdler SS, Sherwood A, et al. High stress responsivity predicts later blood pressure only in combination with positive family history and high life stress. Hypertension. 1999;33:1458
  35. Kirschbaum C, Prussner JC, Stone AA, et al. Persistent high cortisol response to repeated psychological stress in a subpopulation of healthy men. Psychosom Med. 1995;57:468
  36. Moynihan JA. Mechanisms of stress-induced modulation of immunity. Brain Behav Immun. 2003;17(Suppl):S11
  37. Epel ES, Blackburn EH, Lin H, et al. Accelerated telomere shortening in response to life stress. Proc Natl Acad Sci USA. 2004;101:17312
  38. Fawzy FI, Kemeny ME, Fawzy NW, et al. A structured psychiatric intervention for cancer patients. II (Changes over time in immunological measures). Arch Gen Psychiatry. 1990;47:729
  39. Fawzy FI, Canada AL, Fawzy NW. Malignant melanoma: Effects of a brief, structured psychiatric intervention on survival and recurrence at 10-year follow-up. Arch Gen Psychiatry. 2003;60:100
  40. Lanier LL. Natural killer cell receptor signaling. Curr Opin Immunol. 2003;15:308
  41. Sun PD. Structure and function of natural-killer-cell receptors. Immunol Res. 2003;27:539
  42. Farag SS, Fehniger TA, Ruggeri L, et al. Natural killer cell receptors: New biology and insights into the graft-versus-leukemia effect. Blood. 2002;100:1935
  43. Lin Chua H, Brahmi Z. Expression of p58.2 or CD94/NKG2A inhibitory receptors in an NK-like cell line, YTINDY, leads to HLA class I-mediated inhibition of cytotoxicity in the p58.2- but not the CD94/NKG2A-expressing transfectant. Cell Immunol. 2002;219:57
  44. Guerra N, Guillard M, Angevin E, et al. Killer inhibitory receptor (CD158b) modulates the lytic activity of tumor-specific T lymphocytes infiltrating renal cell carcinoma. Blood. 2000;95:2883
  45. Nguyen S, Dhedin N, Vernant JP, et al. VNK-cell reconstitution after haploidentical hematopoietic stem-cell transplantations: Immaturity of NK cells and inhibitory effect of NKG2A override GVL effect. Blood. 2005;105:4135

PII: S0022-4804(06)00483-5

doi: 10.1016/j.jss.2006.08.037

Journal of Surgical Research
Volume 139, Issue 1 , Pages 36-44 , 1 May 2007