The effect of induced hyperthermia on the immune system

Progress in Brain Research

Volumn 162, Issue , 2007, Pages 137-152

  Dieing, Annette ^a   Ahlers, Olaf ^a   Hildebrandt, Bert ^a   Kerner, Thoralf ^a   Tamm, Ingo ^a   Possinger, Kurt ^a   Wust, Peter ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

apoptosis; cytokines; heat shock proteins; lymphocytes; review; stress; whole body hyperthermia

Indexed keywords

HEAT SHOCK PROTEIN; STRESS HORMONE;

APOPTOSIS; CANCER PATIENT; CELL FUNCTION; CELL STIMULATION; CYTOTOXICITY; HEAT; HUMAN; HYPERTHERMIC THERAPY; IMMUNE SYSTEM; IMMUNOLOGY; IMMUNOREGULATION; IN VITRO STUDY; LYMPHOCYTE; MOLECULAR MECHANICS; MONOCYTE; NONHUMAN; PRIORITY JOURNAL; REVIEW; STRESS;

ANIMALS; HUMANS; HYPERTHERMIA, INDUCED; IMMUNE SYSTEM; NEOPLASMS;

EID: 34447629934     PISSN: 00796123     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0079-6123(06)62008-6     Document Type: Review

References (107)

1. Ahlers O., Boehnke T., Kerner T., Deja M., Keh D., Löffel J., Hildebrandt B., Riess H., Wust P., Pappert D., and Gerlach H. Lymphocyte alterations during hyperthermia. Br. J. Anesth. 80 (1998) A 301
2. Ahlers O., Boehnke T., Kerner T., Deja M., Keh D., Löffel J., Hildebrandt B., Riess H., Wust P., Pappert D., and Gerlach H. Changes in serum cytokine levels during induced whole body hyperthermia. Crit. Care 3 (1999) P 082
3. Amaning E.P., and Olszewski W.L. Kinetics of distribution of recirculating lymphocytes during whole body hyperthermia. Arch. Immunol. Ther. Exp. Warsz. 42 (1994) 107-113
4. Ashwell J.D., Lu F.W., and Vacchio M.S. Glucocorticoids in T cell development and function. Annu. Rev. Immunol. 18 (2000) 309-345
5. Atanackovic D., Nierhaus A., Neumeier M., Hossfeld D.K., and Hegewisch-Becker S. 41.8 degrees C whole body hyperthermia as an adjunct to chemotherapy induces prolonged T cell activation in patients with various malignant diseases. Cancer Immunol. Immunother. 51 (2002) 603-613
6. Azocar J., Yunis E.J., and Essex M. Sensitivity of human natural killer cells to hyperthermia. Lancet 1 (1982) 16-17
7. Benschop R.J., Schedlowski M., Wienecke H., Jacobs R., and Schmidt R.E. Adrenergic control of natural killer cell circulation and adhesion. Brain Behav. Immun. 11 (1997) 321-332
8. Blazickova S., Rovensky J., Koska J., and Vigas M. Effect of hyperthermic water bath on parameters of cellular immunity. Int. J. Clin. Pharmacol. Res. 20 (2000) 41-46
9. Borrelli M.J., Calini W.C., Ransom B.R., and Dewey W.C. Ion-sensitive microelectrode measurements of free intracellular chloride and potassium concentrations in hyperthermia-treated neuroblastoma cells. J. Cell Physiol. 126 (1986) 181-190
10. Bouchama A., and Knochel J.P. Heat stroke. N. Engl. J. Med. 346 (2002) 1978-1988
11. Brenner I.K., Zamecnik J., Shek P.N., and Shephard R.J. The impact of heat exposure and repeated exercise on circulating stress hormones. Eur. J. Appl. Physiol. Occup. Physiol. 76 (1997) 445-454
12. Brittenden J., Heys S.D., Ross J., and Eremin O. Natural killer cells and cancer. Cancer 77 (1996) 1226-1243
13. Burd R., Dziedzic T.S., Xu Y., Caliguiri M.A., Subjeck J.R., and Repasky E.A. Tumor cell apoptosis, lymphocyte recruitment and tumor vascular changes are induced by low temperature, long-duration (fever-like) whole-body hyperthermia. J. Cell Physiol. 177 (1998) 137-147
14. Carlson S.L., Fox S., and Abell K.M. Catecholamine modulation of lymphocyte homing to lymphoid tissues. Brain Behav. Immun. 11 (1997) 307-320
15. Coss R.A., and Linnemans W.A. The effects of hyperthermia on the cytoskeleton: a review. Int. J. Hyperthermia 12 (1996) 173-196
16. Delogu G., Famularo G., Moretti S., De Luca A., Tellan G., Antonucci A., Marandola M., and Signore L. Interleukin-10 and apoptotic death of circulating lymphocytes in surgical/anesthesia trauma. J. Trauma 51 (2001) 92-97
17. Delogu G., Moretti S., Famularo G., Antonucci A., Signore L., Marcellini S., Lo Bosco L., and De Simone C. Circulating neutrophils exhibit enhanced apoptosis associated with mitochondrial dysfunctions after surgery under general anaesthesia. Acta Anaesthesiol. Scand. 45 (2001) 87-94
18. Dewey W.C. Mechanism of thermal radiosensitization. In: Urano M., and Douple E. (Eds). Biology of Thermal Potentiation of Radiotherapy (1989), VSP, Utrecht, Tokyo 1-16
19. Dewey W.C. Arrhenius relationships from the molecule and cell to the clinic. Int. J. Hyperthermia 10 (1994) 457-483
20. Dewhirst M.W., Viglianti B.L., Lora-Michiels M., Hanson M., and Hoopes P.J. Basic principles of thermal dosimetry and thermal thresholds for tissue damage from hyperthermia. Int. J. Hyperthermia 19 (2003) 267-294
21. Dhabhar F.S., Miller A.H., McEwen B.S., and Spencer R.L. Stress-induced changes in blood leukocyte distribution. Role of adrenal steroid hormones. J. Immunol. 157 (1996) 1638-1644
22. Dieing A., Ahlers O., Kerner T., Wust P., Felix R., Loffel J., Riess H., and Hildebrandt B. Whole body hyperthermia induces apoptosis in subpopulations of blood lymphocytes. Immunobiology 207 (2003) 265-273
23. Dieing A., Hildebrandt B., Wust P., and Riess H. Differences in hyperthermia-induced programmed cell death in lymphocyte subpopulations in vitro. Immunobiology 203 (2000) E. 4
24. Dinarello C.A., Dempsey R.A., Allegretta M., LoPreste G., Dainiak N., Parkinson D.R., and Mier J.W. Inhibitory effects of elevated temperature on human cytokine production and natural killer activity. Cancer Res. 46 (1986) 6236-6241
25. Dougherty T.F., and Frank J.A. The quantitative and qualitative responses of blood lymphocytes to stress stimuli. J. Lab. Clin. Med. 42 (1953) 530-537
26. Downing J.F., Martinez-Valdez H., Elizondo R.S., Walker E.B., and Taylor M.W. Hyperthermia in humans enhances interferon-gamma synthesis and alters the peripheral lymphocyte population. J. Interferon Res. 8 (1988) 143-150
27. Edwards M.J., Saunders R.D., and Shiota K. Effects of heat on embryos and foetuses. Int. J. Hyperthermia 19 (2003) 295-324
28. Eichhorst S.T., Muerkoster S., Weigand M.A., and Krammer P.H. The chemotherapeutic drug 5-fluorouracil induces apoptosis in mouse thymocytes in vivo via activation of the CD95(APO-1/Fas) system. Cancer Res. 61 (2001) 243-248
29. Elenkov I.J. Glucocorticoids and the Th1/Th2 balance. Ann. N.Y. Acad. Sci. 1024 (2004) 138-146
30. Elenkov I.J., and Chrousos G.P. Stress hormones, proinflammatory and antiinflammatory cytokines, and autoimmunity. Ann. N.Y. Acad. Sci. 966 (2002) 290-303
31. Evans S.S., Wang W.C., Bain M.D., Burd R., Ostberg J.R., and Repasky E.A. Fever-range hyperthermia dynamically regulates lymphocyte delivery to high endothelial venules. Blood 97 (2001) 2727-2733
32. Faithfull N.S., Reinhold H.S., Berg A.P.V.D., Rhoon G.C.V., Zee J.V.D., and Wike-Hooley J.L. Cardiovascular changes during whole body hyperthermia treatment of advanced malignancy. Eur. J. Appl. Physiol. 53 (1984) 274-281
33. Frankfurt O., and Rosen S.T. Mechanisms of glucocorticoid-induced apoptosis in hematologic malignancies: updates. Curr. Opin. Oncol. 16 (2004) 553-563
34. Furuke K., Burd P.R., Horvath-Arcidiacono J.A., Hori K., Mostowski H., and Bloom E.T. Human NK cells express endothelial nitric oxide synthase, and nitric oxide protects them from activation-induced cell death by regulating expression of TNF-alpha. J. Immunol. 163 (1999) 1473-1480
35. Galon J., Franchimont D., Hiroi N., Frey G., Boettner A., Ehrhart-Bornstein M., O'Shea J.J., Chrousos G.P., and Bornstein S.R. Gene profiling reveals unknown enhancing and suppressive actions of glucocorticoids on immune cells. FASEB J. 16 (2002) 61-71
36. Gehrmann M., Marienhagen J., Eichholtz-Wirth H., Fritz E., Ellwart J., Jaattela M., Zilch T., and Multhoff G. Dual function of membrane-bound heat shock protein 70 (Hsp70), Bag-4, and Hsp40: protection against radiation-induced effects and target structure for natural killer cells. Cell Death Differ. 12 (2005) 38-51
37. Hammami M.M., Bouchama A., Shail E., Aboul-Enein H.Y., and Al-Sedairy S. Lymphocyte subsets and adhesion molecules expression in heatstroke and heat stress. J. Appl. Physiol. 84 5 (1998) 1615-1621
38. Haveman J., Geerdink A.G., and Rodermond H.M. Cytokine production after whole body and localized hyperthermia. Int. J. Hyperthermia 12 (1996) 791-800
39. Hegewisch-Becker S., Nierhaus A., Panse J., Wiedenmann G., and Hossfeld D.K. Whole body hyperthermia has a stimulatory effect on the immune cell activity in cancer patients. Ann. Oncol. 9 Suppl 4 (1998) 136-137
40. Hellstrand K., and Hermodsson S. An immunopharmacological analysis of adrenaline-induced suppression of human natural killer cell cytotoxicity. Int. Arch. Allergy Appl. Immunol. 89 (1989) 334-341
41. Hildebrandt B., Hegewisch-Becker S., Kerner T., Nierhaus A., Bakhshandeh-Bath A., Janni W., Zumschlinge R., Sommer H., Riess H., and Wust P. Current status of radiant whole-body hyperthermia at temperatures >41.5 degrees C and practical guidelines for the treatment of adults. The German 'Interdisciplinary Working Group on Hyperthermia'. Int. J. Hyperthermia 21 (2005) 169-183
42. Hildebrandt B., Wust P., Ahlers O., Dieing A., Sreenivasa G., Kerner T., Felix R., and Riess H. The cellular and molecular basis of hyperthermia. Crit. Rev. Oncol./Hematol. 43 (2002) 33-56
43. Ida H., and Anderson P. Activation-induced NK cell death triggered by CD2 stimulation. Eur. J. Immunol. 28 (1998) 1292-1300
44. Ida H., Nakashima T., Kedersha N.L., Yamasaki S., Huang M., Izumi Y., Miyashita T., Origuchi T., Kawakami A., Migita K., Bird P.I., Anderson P., and Eguchi K. Granzyme B leakage-induced cell death: a new type of activation-induced natural killer cell death. Eur. J. Immunol. 33 (2003) 3284-3292
45. Iwakabe K., Shimada M., Ohta A., Yahata T., Ohmi Y., Habu S., and Nishimura T. The restraint stress drives a shift in Th1/Th2 balance toward Th2-dominant immunity in mice. Immunol. Lett. 62 (1998) 39-43
46. Jaattelä M. Heat shock proteins as cellular lifeguards. Ann. Med. 31 (1999) 261-271
47. Janeway, C.A., Travers, P., Walport, M. and Shlomchik, M. (2001) Develpoment and survival of lymphocytes. In: Immunobiology: The Immune System in Health and Disease. Garland Science, New York.
48. Jolly C., and Morimoto R.I. Role of the heat shock response and molecular chaperones in oncogenesis and cell death. J. Natl. Cancer Inst. 92 (2000) 1564-1572
49. Kalland T., and Dahlquist I. Effects of in vitro hyperthermia on human natural killer cells. Cancer Res. 43 (1983) 1842-1846
50. Kampinga H.H., Dynlacht J.R., and Dikomey E. Mechanism of radiosensitization by hyperthermia (> or =43 degrees C) as derived from studies with DNA repair defective mutant cell lines. Int. J. Hyperthermia 20 (2004) 131-139
51. Kappel M., Stadeager C., Tvede N., Galbo H., and Pedersen B.K. Effects of in vivo hyperthermia on natural killer cell activity, in vitro proliferative responses and blood mononuclear cell subpopulations. Clin. Exp. Immunol. 84 (1991) 175-180
52. Katschinski D., Wiedemann G.J., Longo W., d'Oleire F.R., Spriggs D., and Robins H.I. Whole body hyperthermia cytokine induction: a review, and unifying hypothesis for myeloprotection in the setting of cytotoxic therapy. Cytokine Growth Factor Rev. 10 (1999) 93-97
53. Kearns R.J., Ringler S., Krakowka S., Tallman R., Sites J., and Oglesbee M.J. The effects of extracorporal whole body hyperthermia on the functional and phenotypic features of canine peripheral blood mononuclear cells (PBMC). Clin. Exp. Immunol. 116 (1999) 188-192
54. Kerner T., Deja M., Ahlers O., Loffel J., Hildebrandt B., Wust P., Gerlach H., and Riess H. Whole body hyperthermia: a secure procedure for patients with various malignancies?. Intensive Care Med. 25 (1999) 959-965
55. Kerner T., Hildebrandt B., Ahlers O., Deja M., Riess H., Draeger J., Wust P., and Gerlach H. Anaesthesiological experiences with whole body hyperthermia. Int. J. Hyperthermia 19 (2003) 1-12
56. Klokker M., Secher N.H., Madsen P., Pedersen M., and Pedersen B.K. Adrenergic beta1- and beta1+2-receptor blockade suppress the natural killer cell response to head-up tilt in humans. J. Appl. Physiol. 83 5 (1997) 1492-1498
57. Kohm A.P., and Sanders V.M. Norepinephrine and beta 2-adrenergic receptor stimulation regulate CD4+ T and B lymphocyte function in vitro and in vivo. Pharmacol. Rev. 53 (2001) 487-525
58. Krause S.W., Gastpar R., Andreesen R., Gross C., Ullrich H., Thonigs G., Pfister K., and Multhoff G. Treatment of colon and lung cancer patients with ex vivo heat shock protein 70-peptide-activated, autologous natural killer cells: a clinical phase I trial. Clin. Cancer Res. 10 (2004) 3699-3707
59. Kraybill W.G., Olenki T., Evans S.S., Ostberg J.R., O'Leary K.A., Gibbs J.F., and Repasky E.A. A phase I study of fever-range whole body hyperthermia (FR-WBH) in patients with advanced solid tumours: correlation with mouse models. Int. J. Hyperthermia 18 (2002) 253-266
60. Kregel K.C. Heat shock proteins: modifying factors in physiological stress response and acquired thermotolerance. J. Appl. Physiol. 92 (2002) 2177-2186
61. Krueger A., Fas S.C., Baumann S., and Krammer P.H. The role of CD95 in the regulation of peripheral T-cell apoptosis. Immunol. Rev. 193 (2003) 58-69
62. Leite-de-Moraes M.C., Herbelin A., Gouarin C., Koezuka Y., Schneider E., and Dy M. Fas/Fas ligand interactions promote activation-induced cell death of NK T lymphocytes. J. Immunol. 165 (2000) 4367-4371
63. Lepock J.R. Cellular effects of hyperthermia: relevance to the minimum dose for thermal damage. Int. J. Hyperthermia 19 (2003) 252-266
64. Li C.Y., and Dewhirst M.W. Hyperthermia-regulated immunogene therapy. Int. J. Hyperthermia 18 (2002) 586-596
65. Madden K.S., Sanders V.M., and Felten D.L. Catecholamine influences and sympathetic neural modulation of immune responsiveness. Annu. Rev. Pharmacol. Toxicol. 35 (1995) 417-448
66. Migita K., Eguchi K., Kawabe Y., Nakamura T., Shirabe S., Tsukada T., Ichinose Y., Nakamura H., and Nagataki S. Apoptosis induction in human peripheral blood T lymphocytes by high-dose steroid therapy. Transplantation 63 (1997) 583-587
67. Migliorati G., Pagliacci C., Moraca R., Crocicchio F., Nicoletti I., and Riccardi C. Glucocorticoid-induced apoptosis of natural killer cells and cytotoxic T lymphocytes. Pharmacol. Res. 26 Suppl 2 (1992) 26-27
68. Milani V., Noessner E., Ghose S., Kuppner M., Ahrens B., Scharner A., Gastpar R., and Issels R.D. Heat shock protein 70: role in antigen presentation and immune stimulation. Int. J. Hyperthermia 18 (2002) 563-575
69. Multhoff G. Activation of natural killer cells by heat shock protein 70. Int. J. Hyperthermia 18 (2002) 576-585
70. Myerson R.J., Roti Roti J.L., Moros E.G., Straube W.L., and Xu M. Modelling heat-induced radiosensitization: clinical implications. Int. J. Hyperthermia 20 (2004) 201-212
71. Onsrud M. Effect of hyperthermia on human natural killer cells. Recent Results Cancer Res. 109 (1988) 50-56
72. Ortaldo J.R., Mason A.T., and O'Shea J.J. Receptor-induced death in human natural killer cells: involvement of CD16. J. Exp. Med. 181 (1995) 339-344
73. Ostberg J.R., Kaplan K.C., and Repasky E.A. Induction of stress proteins in a panel of mouse tissues by fever-range whole body hyperthermia. Int. J. Hyperthermia 18 (2002) 552-562
74. Pedersen B.K., and Hoffman-Goetz L. Exercise and the immune system: regulation, integration, and adaptation. Physiol. Rev. 80 (2000) 1055-1081
75. Planey S.L., and Litwack G. Glucocorticoid-induced apoptosis in lymphocytes. Biochem. Biophys. Res. Commun. 279 (2000) 307-312
76. Provinciali M., Ciavattini A., Di-Stefano G., Argentati K., and Garzetti G.G. In vivo amifostine (WR-2721) prevents chemotherapy-induced apoptosis of peripheral blood lymphocytes from cancer patients. Life Sci. 64 (1999) 1525-1532
77. Rathmell J.C., and Thompson C.B. Pathways of apoptosis in lymphocyte development, homeostasis, and disease. Cell 109 Suppl (2002) S97-S107
78. Repasky E., and Issels R. Physiological consequences of hyperthermia: heat, heat shock proteins and the immune response. Int. J. Hyperthermia 18 (2002) 486-489
79. Rhind S.G., Gannon G.A., Shephard R.J., Buguet A., Shek P.N., and Radomski M.W. Cytokine induction during exertional hyperthermia is abolished by core temperature clamping: neuroendocrine regulatory mechanisms. Int. J. Hyperthermia 20 (2004) 503-516
80. Robertson M.J., and Ritz J. Biology and clinical relevance of human natural killer cells. Blood 76 (1990) 2421-2438
81. Robins H.I., Kalin N.H., Shelton S.E., Martin P.A., Shecterle L.M., Barksdale C.M., Neville A.J., and Marshall J. Rise in plasma beta-endorphin, ACTH, and cortisol in cancer patients undergoing whole body hyperthermia. Horm. Metab. Res. 19 (1987) 441-443
82. Robins H.I., Kalin N.H., Shelton S.E., Shecterle L.M., Barksdale C.M., Martin P.A., and Marshall J. Neuroendocrine changes in patients undergoing whole body hyperthermia. Int. J. Hyperthermia 3 (1987) 99-105
83. Robins H.I., Kutz M., Wiedemann G.J., Katschinski D.M., Paul D., Grosen E., Tiggelaar C.L., Spriggs D., Gillis W., and d'Oleire F. Cytokine induction by 41.8°C whole body hyperthermia. Cancer Lett. 97 (1995) 195-201
84. Romanovsky A.A., and Blatteis C.M. Pathophysiology of opioids in hyperthermic states. Prog. Brain Res. 115 (1998) 111-127
85. Sakaguchi Y., Stephens L.C., Makino M., Kaneko T., Strebel F.R., Danhauser L.L., Jenkins G.N., and Bull J.M. Apoptosis in tumors and normal tissues induced by whole body hyperthermia in rats. Cancer Res. 55 (1995) 5459-5464
86. Sasajima K., Inokuchi K., Onda M., Miyashita M., Okawa K.I., Matsutani T., and Takubo K. Detection of T cell apoptosis after major operations. Eur. J. Surg. 165 (1999) 1020-1023
87. Schedlowski M., Hosch W., Oberbeck R., Benschop R.J., Jacobs R., Raab H.R., and Schmidt R.E. Catecholamines modulate human NK cell circulation and function via spleen-independent beta 2-adrenergic mechanisms. J. Immunol. 156 (1996) 93-99
88. Schroeder S., Lindemann C., Decker D., Klaschik S., Hering R., Putensen C., Hoeft A., von Ruecker A., and Stuber F. Increased susceptibility to apoptosis in circulating lymphocytes of critically ill patients. Langenbecks Arch. Surg. 386 (2001) 42-46
89. Shah A., Unger E., Bain M.D., Bruce R., Bodkin J., Ginnetti J., Wang W.C., Seon B., Stewart C.C., and Evans S.S. Cytokine and adhesion molecule expression in primary human endothelial cells stimulated with fever-range hyperthermia. Int. J. Hyperthermia 18 (2002) 534-551
90. Sharma H.S., and Hoopes P.J. Hyperthermia induced pathophysiology of the central nervous system. Int. J. Hyperthermia 19 (2003) 325-354
91. Shen R.N., Lu L., Young P., Shidnia H., Hornback N.B., and Broxmeyer H.E. Influence of elevated temperature on natural killer cell activity, lymphokine-activated killer cell activity and lectin-dependent cytotoxicity of human umbilical cord blood and adult blood cells. Int. J. Radiat. Oncol. Biol. Phys. 29 (1994) 821-826
92. Shi Y., Devadas S., Greeneltch K.M., Yin D., Allan Mufson R., and Zhou J.N. Stressed to death: implication of lymphocyte apoptosis for psychoneuroimmunology. Brain Behav. Immun. 17 Suppl 1 (2003) S18-S26
93. Srivastava P. Roles of heat-shock proteins in innate and adaptive immunity. Nat. Rev. Immunol. 2 (2002) 185-194
94. Stahnke K., Fulda S., Friesen C., Strauss G., and Debatin K.M. Activation of apoptosis pathways in peripheral blood lymphocytes by in vivo chemotherapy. Blood 98 (2001) 3066-3073
95. Strasser A., and Bouillet P. The control of apoptosis in lymphocyte selection. Immunol. Rev. 193 (2003) 82-92
96. Tsan M.F., and Gao B. Cytokine function of heat shock proteins. Am. J. Physiol. Cell Physiol. 286 (2004) C739-C744
97. Van Den Brande J.M., Peppelenbosch M.P., and Van Deventer S.J. Treating Crohn's disease by inducing T lymphocyte apoptosis. Ann. N.Y. Acad. Sci. 973 (2002) 166-180
98. Vidair C., and Dewey W.C. Two distinct modes of hyperthermic death. Radiat. Res. 116 (1988) 157-171
99. Vujaskovic Z., and Song C.W. Physiological mechanisms underlying heat-induced radiosensitization. Int. J. Hyperthermia 20 (2004) 163-174
100. Wang J., Charboneau R., Barke R.A., Loh H.H., and Roy S. Mu-opioid receptor mediates chronic restraint stress-induced lymphocyte apoptosis. J. Immunol. 169 (2002) 3630-3636
101. Woiciechowsky C., Asadullah K., Nestler D., Eberhardt B., Platzer C., Schoening B., Gloeckner F., Lanksch W.R., Volk H.D., and Doecke W.D. Sympathetic activation triggers systemic interleukin-10 release in immunodepression induced by brain injury. Nat. Med. 4 (1998) 808-813
102. Wust P., Hildebrandt B., Sreenivasa G., Rau B., Gellermann J., Riess H., Felix R., and Schlag P.M. Hyperthermia in combined treatment of cancer. Lancet Oncol. 3 (2002) 487-497
103. Xia Z., DePierre J.W., and Nassberger L. Dysregulation of bcl-2, c-myc, and Fas expression during tricyclic antidepressant-induced apoptosis in human peripheral lymphocytes. J. Biochem. Toxicol. 11 (1996) 203-204
104. Yang H., Lauzon W., and Lemaire I. Effects of hyperthermia on natural killer cells: inhibition of lytic function and microtubule organization. Int. J. Hyperthermia 8 (1992) 87-97
105. Yonezawa M., Otsuka T., Matsui N., Tsuji H., et al. Hyperthermia induces apoptosis in malignant fibrous histiocytoma cells in vitro. Int. J. Cancer 66 (1996) 347-351
106. van der Zee J. Heating the patient: a promising approach?. Ann. Oncol. 13 (2002) 1173-1184
107. Zellner M., Hergovics N., Roth E., Jilma B., Spittler A., and Oehler R. Human monocyte stimulation by experimental whole body hyperthermia. Wien Klin Wochenschr 114 (2002) 102-107