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Original

Targeted regulation of a lymphocyte-endothelial-interleukin-6 axis by thermal stress

, , &
Pages 67-78 | Received 10 Oct 2007, Accepted 28 Oct 2007, Published online: 09 Jul 2009

References

  • Gattinoni L, Powell Jr DJ, Rosenberg SA, Restifo NP. Adoptive immunotherapy for cancer: Building on success. Nat Rev Immunol 2006; 6: 383–393
  • Dudley ME, Rosenberg SA. Adoptive-cell-transfer therapy for the treatment of patients with cancer. Nat Rev Cancer 2003; 3: 666–675
  • Boon T, Coulie PG, Eynde BJ, Bruggen PV. Human T cell responses against melanoma. Annu Rev Immunol 2006; 24: 175–208
  • Pardoll DM. Spinning molecular immunology into successful immunotherapy. Nat Rev Immunol 2002; 2: 227–238
  • Ho WY, Blattman JN, Dossett ML, Yee C, Greenberg PD. Adoptive immunotherapy: Engineering T cell responses as biologic weapons for tumor mass destruction. Cancer Cell 2003; 3: 431–437
  • June CH. Adoptive T cell therapy for cancer in the clinic. J Clin Invest 2007; 117: 1466–1476
  • Harty JT, Tvinnereim AR, White DW. CD8+ T cell effector mechanisms in resistance to infection. Annu Rev Immunol 2000; 18: 275–308
  • Gajewski TF, Meng Y, Blank C, Brown I, Kacha A, Kline J, Harlin H. Immune resistance orchestrated by the tumor microenvironment. Immunol Rev 2006; 213: 131–145
  • Cochran AJ, Huang RR, Lee J, Itakura E, Leong SP, Essner R. Tumour-induced immune modulation of sentinel lymph nodes. Nat Rev Immunol 2006; 6: 659–670
  • Butcher EC, Picker LJ. Lymphocyte homing and homeostasis. Science 1996; 272(5258)60–66
  • von Andrian UH, Mempel TR. Homing and cellular traffic in lymph nodes. Nat Rev Immunol 2003; 3: 867–878
  • Engelhardt B, Wolburg H. Mini-review: Transendothelial migration of leukocytes: Through the front door or around the side of the house?. Eur J Immunol 2004; 34: 2955–2963
  • Chen Q, Clancy KA, Wang WC, Evans SS. Inflammatory cues controlling lymphocyte-endothelial interactions during fever-range thermal stress. Endothelial Biomedicine, W Aird. Cambridge University Press, Cambridge 2007
  • von Andrian UH. Intravital microscopy of the peripheral lymph node microcirculation in mice. Microcirculation 1996; 3: 287–300
  • Pabst R, Binns RM. Heterogeneity of lymphocyte homing physiology: Several mechanisms operate in the control of migration to lymphoid and non-lymphoid organs in vivo. Immunol Rev 1989; 108: 83–109
  • Blattman JN, Antia R, Sourdive DJ, Wang X, Kaech SM, Murali-Krishna K, Altman JD, Ahmed R. Estimating the precursor frequency of naive antigen-specific CD8 T cells. J Exp Med 2002; 195: 657–664
  • Zou W. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer 2005; 5: 263–274
  • Gabrilovich D. Mechanisms and functional significance of tumour-induced dendritic-cell defects. Nat Rev Immunol 2004; 4: 941–952
  • Sica A, Bronte V. Altered macrophage differentiation and immune dysfunction in tumor development. J Clin Invest 2007; 117: 1155–1166
  • Carriere V, Colisson R, Jiguet-Jiglaire C, Bellard E, Bouche G, Al Saati T, Amalric F, Girard JP, M'Rini C. Cancer cells regulate lymphocyte recruitment and leukocyte-endothelium interactions in the tumor-draining lymph node. Cancer Res 2005; 65: 11639–1148
  • Rosenberg SA, Yang JC, Restifo NP. Cancer immunotherapy: Moving beyond current vaccines. Nat Med 2004; 10(9)909–915
  • Springer TA. Traffic signals for lymphocyte recirculation and leukocyte emigration: The multistep paradigm. Cell 1994; 76: 301–314
  • Chen Q, Fisher DT, Kucinska SA, Wang WC, Evans SS. Dynamic control of lymphocyte trafficking by fever-range thermal stress. Cancer Immunol Immunother 2006; 55: 299–311
  • Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages C, Tosolini M, Camus M, Berger A, Wind P, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006; 313: 1960–1964
  • Chen Q, Wang WC, Evans SS. Tumor microvasculature as a barrier to antitumor immunity. Cancer Immunol Immunother 2003; 52: 670–679
  • Fisher DT, Chen Q, Appenheimer MM, Skitzki J, Wang WC, Odunsi K, Evans SS. Hurdles to lymphocyte trafficking in the tumor microenvironment: Implications for effective immunotherapy. Immunol Invest 2006; 35: 251–277
  • Yamshchikov GV, Mullins DW, Chang CC, Ogino T, Thompson L, Presley J, Galavotti H, Aquila W, Deacon D, Ross W, et al. Sequential immune escape and shifting of T cell responses in a long-term survivor of melanoma. J Immunol 2005; 174: 6863–6871
  • Yamshchikov G, Thompson L, Ross WG, Galavotti H, Aquila W, Deacon D, Caldwell J, Patterson JW, Hunt DF, Slingluff CL, Jr. Analysis of a natural immune response against tumor antigens in a melanoma survivor: Lessons applicable to clinical trial evaluations. Clin Cancer Res 2001; 7(Suppl 3)S909–S916
  • Skitzki J, Muhitch J, Evans SS. Tracking the elusive lymphocyte: Methods of detection during adoptive immunotherapy. Immunol Invest in press
  • McDonald DM, Choyke PL. Imaging of angiogenesis: From microscope to clinic. Nat Med 2003; 9: 713–725
  • Jain RK, Munn LL, Fukumura D. Dissecting tumour pathophysiology using intravital microscopy. Nat Rev Cancer 2002; 2: 266–276
  • Springer TA. Traffic signals on endothelium for lymphocyte recirculation and leukocyte emigration. Annu Rev Physiol 1995; 57: 827–872
  • Kubes P, Kanwar S. Histamine induces leukocyte rolling in post-capillary venules. A P-selectin-mediated event. J Immunol 1994; 152: 3570–3577
  • McDonald DM, Thurston G, Baluk P. Endothelial gaps as sites for plasma leakage in inflammation. Microcirculation 1999; 6: 7–22
  • Ley K. Integration of inflammatory signals by rolling neutrophils. Immunol Rev 2002; 186: 8–18
  • Luster AD, Alon R, von Andrian UH. Immune cell migration in inflammation: Present and future therapeutic targets. Nat Immunol 2005; 6: 1182–1190
  • McDonald DM. Imaging of angiogenesis in inflammation and cancer: Lessons for novel treatment of allergic rhinitis. Clin Exp Allergy Rev 2007; 7: 11–18
  • McDonald DM, Foss AJ. Endothelial cells of tumor vessels: Abnormal but not absent. Cancer Metastasis Rev 2000; 19: 109–120
  • Appenheimer MM, Chen Q, Girard RA, Wang WC, Evans SS. Impact of fever-range thermal stress on lymphocyte-endothelial adhesion and lymphocyte trafficking. Immunol Invest 2005; 34: 295–323
  • Chen Q, Fisher DT, Clancy KA, Gauguet JM, Wang WC, Unger E, Rose-John S, von Andrian UH, Baumann H, Evans SS. Fever-range thermal stress promotes lymphocyte trafficking across high endothelial venules via an interleukin 6 trans-signaling mechanism. Nat Immunol 2006; 7: 1299–1308
  • Hansson GK. Immune mechanisms in atherosclerosis. Arterioscler Thromb Vasc Biol 2001; 21: 1876–1890
  • Chen Q, Evans SS. Thermal regulation of lymphocyte trafficking: Hot spots of the immune response. Int J Hyperthermia 2005; 21(8)723–729
  • Ganss R, Ryschich E, Klar E, Arnold B, Hammerling GJ. Combination of T-Cell therapy and trigger of inflammation induces remodeling of the vasculature and tumor eradication. Cancer Res 2002; 62: 1462–1470
  • Onrust SV, Hartl PM, Rosen SD, Hanahan D. Modulation of L-selectin ligand expression during an immune response accompanying tumorigenesis in transgenic mice. J Clin Invest 1996; 97: 54–64
  • Carlos TM. Leukocyte recruitment at sites of tumor: Dissonant orchestration. J Leukoc Biol 2001; 70: 171–184
  • Ganss R, Arnold B, Hammerling GJ. Mini-review: Overcoming tumor-intrinsic resistance to immune effector function. Eur J Immunol 2004; 34: 2635–2641
  • Gollnick SO, Evans SS, Baumann H, Owczarczak B, Maier P, Vaughan L, Wang WC, Unger E, Henderson BW. Role of cytokines in photodynamic therapy-induced local and systemic inflammation. Br J Cancer 2003; 88: 1772–1779
  • Lugade AA, Moran JP, Gerber SA, Rose RC, Frelinger JG, Lord EM. Local radiation therapy of B16 melanoma tumors increases the generation of tumor antigen-specific effector cells that traffic to the tumor. J Immunol 2005; 174: 7516–7523
  • Weishaupt C, Munoz KN, Buzney E, Kupper TS, Fuhlbrigge RC. T-cell distribution and adhesion receptor expression in metastatic melanoma. Clin Cancer Res 2007; 13: 2549–2556
  • Piali L, Fichtel A, Terpe HJ, Imhof BA, Gisler RH. Endothelial vascular cell adhesion molecule 1 expression is suppressed by melanoma and carcinoma. J Exp Med 1995; 181: 811–816
  • Kunkel EJ, Butcher EC. Chemokines and the tissue-specific migration of lymphocytes. Immunity 2002; 16: 1–4
  • Wu NZ, Klitzman B, Dodge R, Dewhirst MW. Diminished leukocyte-endothelium interaction in tumor microvessels. Cancer Res 1992; 52: 4265–4268
  • Ryschich E, Schmidt J, Hammerling GJ, Klar E, Ganss R. Transformation of the microvascular system during multistage tumorigenesis. Int J Cancer 2002; 97: 719–725
  • Hellebrekers DM, Castermans K, Vire E, Dings RP, Hoebers NT, Mayo KH, Oude Egbrink MG, Molema G, Fuks F, van Engeland M, Griffioen AW. Epigenetic regulation of tumor endothelial cell anergy: Silencing of intercellular adhesion molecule-1 by histone modifications. Cancer Res 2006; 66: 10770–10777
  • Bessa X, Elizalde JI, Mitjans F, Pinol V, Miquel R, Panes J, Piulats J, Pique JM, Castells A. Leukocyte recruitment in colon cancer: Role of cell adhesion molecules, nitric oxide, and transforming growth factor beta1. Gastroenterology 2002; 122: 1122–1132
  • Ley K, Laudanna C, Cybulsky MI, Nourshargh S. Getting to the site of inflammation: The leukocyte adhesion cascade updated. Nat Rev Immunol 2007; 7: 678–689
  • Fukumura D, Salehi HA, Witwer B, Tuma RF, Melder RJ, Jain RK. Tumor necrosis factor alpha-induced leukocyte adhesion in normal and tumor vessels: Effect of tumor type, transplantation site, and host strain. Cancer Res 1995; 55: 4824–4829
  • Melder RJ, Koenig GC, Witwer BP, Safabakhsh N, Munn LL, Jain RK. During angiogenesis, vascular endothelial growth factor and basic fibroblast growth factor regulate natural killer cell adhesion to tumor endothelium. Nat Med 1996; 2: 992–997
  • Griffioen AW, Damen CA, Martinotti S, Blijham GH, Groenewegen G. Endothelial intercellular adhesion molecule-1 expression is suppressed in human malignancies: The role of angiogenic factors. Cancer Res 1996; 56: 1111–1117
  • Dirkx AE, Oude Egbrink MG, Kuijpers MJ, van der Niet ST, Heijnen VV, Bouma-ter Steege JC, Wagstaff J, Griffioen AW. Tumor angiogenesis modulates leukocyte-vessel wall interactions in vivo by reducing endothelial adhesion molecule expression. Cancer Res 2003; 63: 2322–2329
  • Bouma-ter Steege JC, Baeten CI, Thijssen VL, Satijn SA, Verhoeven IC, Hillen HF, Wagstaff J, Griffioen AW. Angiogenic profile of breast carcinoma determines leukocyte infiltration. Clin Cancer Res 2004; 10: 7171–7178
  • Skitzki J, Craig RA, Okuyama R, Knibbs RN, McDonagh K, Chang AE, Stoolman LM. Donor cell cycling, trafficking, and accumulation during adoptive immunotherapy for murine lung metastases. Cancer Res 2004; 64: 2183–2191
  • Skitzki JJ, Chen Q, Wang WC, Evans SS. Primary immune surveillance: Some like it hot. J Mol Med 2007; 85: 1361–1367
  • Palmer DC, Balasubramaniam S, Hanada K, Wrzesinski C, Yu Z, Farid S, Theoret MR, Hwang LN, Klebanoff CA, Gattinoni L, et al. Vaccine-stimulated, adoptively transferred CD8+ T cells traffic indiscriminately and ubiquitously while mediating specific tumor destruction. J Immunol 2004; 173: 7209–7216
  • Rosenberg SA, Sherry RM, Morton KE, Scharfman WJ, Yang JC, Topalian SL, Royal RE, Kammula U, Restifo NP, Hughes MS, et al. Tumor progression can occur despite the induction of very high levels of self/tumor antigen-specific CD8+ T cells in patients with melanoma. J Immunol 2005; 175: 6169–6176
  • Nestle FO, Alijagic S, Gilliet M, Sun Y, Grabbe S, Dummer R, Burg G, Schadendorf D. Vaccination of melanoma patients with peptide- or tumor lysate-pulsed dendritic cells. Nat Med 1998; 4: 328–332
  • Banchereau J, Palucka AK, Dhodapkar M, Burkeholder S, Taquet N, Rolland A, Taquet S, Coquery S, Wittkowski KM, Bhardwaj N, et al. Immune and clinical responses in patients with metastatic melanoma to CD34(+) progenitor-derived dendritic cell vaccine. Cancer Res 2001; 61: 6451–6458
  • Overwijk WW, Theoret MR, Finkelstein SE, Surman DR, de Jong LA, Vyth-Dreese FA, Dellemijn TA, Antony PA, Spiess PJ, Palmer DC, et al. Tumor regression and autoimmunity after reversal of a functionally tolerant state of self-reactive CD8+ T cells. J Exp Med 2003; 198: 569–580
  • Vardam TD, Zhou L, Appenheimer MM, Chen Q, Wang WC, Baumann H, Evans SS. Regulation of the lymphocyte–endothelial–IL-6 axis by fever-range thermal stress: Hot spot of immune surveillance cytokine. 2007; 39: 84–96
  • Wherry EJ, Teichgraber V, Becker TC, Masopust D, Kaech SM, Antia R, von Andrian UH, Ahmed R. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat Immunol 2003; 4: 225–234
  • Huang J, Khong HT, Dudley ME, El-Gamil M, Li YF, Rosenberg SA, Robbins PF. Survival, persistence, and progressive differentiation of adoptively transferred tumor-reactive T cells associated with tumor regression. J Immunother (1997) 2005; 28: 258–267
  • Gattinoni L, Klebanoff CA, Palmer DC, Wrzesinski C, Kerstann K, Yu Z, Finkelstein SE, Theoret MR, Rosenberg SA, Restifo NP. Acquisition of full effector function in vitro paradoxically impairs the in vivo antitumor efficacy of adoptively transferred CD8+ T cells. J Clin Invest 2005; 115: 1616–1626
  • Appenheimer MM, Girard RA, Chen Q, Wang WC, Bankert KC, Hardison J, Bain MD, Ridgley F, Sarcione EJ, S. B, Kaspers B, et al. Conservation of IL-6 trans-signaling mechanisms controlling L-selectin adhesion by fever-range thermal stress. Eur J Immunol 2007; 37: 2856–2867
  • Wang WC, Goldman LM, Schleider DM, Appenheimer MM, Subjeck JR, Repasky EA, Evans SS. Fever-range hyperthermia enhances L-selectin-dependent adhesion of lymphocytes to vascular endothelium. J Immunol 1998; 160: 961–969
  • Evans SS, Schleider DM, Bowman LA, Francis ML, Kansas GS, Black JD. Dynamic association of L-selectin with the lymphocyte cytoskeletal matrix. J Immunol 1999; 162: 3615–3624
  • Evans SS, Bain MD, Wang WC. Fever-range hyperthermia stimulates alpha4beta7 integrin-dependent lymphocyte-endothelial adhesion. Int J Hyperthermia 2000; 16: 45–59
  • Evans SS, Wang WC, Bain MD, Burd R, Ostberg JR, Repasky EA. Fever-range hyperthermia dynamically regulates lymphocyte delivery to high endothelial venules. Blood 2001; 97: 2727–2733
  • Chen Q, Wang WC, Bruce R, Li H, Schleider DM, Mulbury MJ, Bain MD, Wallace PK, Baumann H, Evans SS. Central role of IL-6 receptor signal-transducing chain gp130 in activation of L-selectin adhesion by fever-range thermal stress. Immunity 2004; 20: 59–70
  • Pavalko FM, Walker DM, Graham L, Goheen M, Doerschuk CM, Kansas GS. The cytoplasmic domain of L-selectin interacts with cytoskeletal proteins via alpha-actinin: Receptor positioning in microvilli does not require interaction with alpha-actinin. J Cell Biol 1995; 129: 1155–1164
  • Burd R, Dziedzic TS, Xu Y, Caligiuri MA, Subjeck JR, Repasky EA. Tumor cell apoptosis, lymphocyte recruitment and tumor vascular changes are induced by low temperature, long duration (fever-like) whole body hyperthermia. J Cell Physiol 1998; 177: 137–147
  • Kraybill WG, Olenki T, Evans SS, Ostberg JR, O'Leary KA, Gibbs JF, Repasky EA. 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 2002; 18: 253–266
  • Ostberg JR, Gellin C, Patel R, Repasky EA. Regulatory potential of fever-range whole body hyperthermia on Langerhans cells and lymphocytes in an antigen-dependent cellular immune response. J Immunol 2001; 167: 2666–2670
  • Ostberg JR, Repasky EA. Comparison of the effects of two different whole body hyperthermia protocols on the distribution of murine leukocyte populations. Int J Hyperthermia 2000; 16: 29–43
  • Pritchard MT, Ostberg JR, Evans SS, Burd R, Kraybill W, Bull JM, Repasky EA. Protocols for simulating the thermal component of fever: Preclinical and clinical experience. Methods 2004; 32: 54–62
  • Tedla N, Wang HW, McNeil HP, Di Girolamo N, Hampartzoumian T, Wakefield D, Lloyd A. Regulation of T lymphocyte trafficking into lymph nodes during an immune response by the chemokines macrophage inflammatory protein (Mip)-1α alpha and Mip-1β beta. J Immunol 1998; 161: 5663–5672
  • Mackay CR, Marston W, Dudler L. Altered patterns of T cell migration through lymph nodes and skin following antigen challenge. Eur J Immunol 1992; 22: 2205–2210
  • Guarda G, Hons M, Soriano SF, Huang AY, Polley R, Martin-Fontecha A, Stein JV, Germain RN, Lanzavecchia A, Sallusto F. L-selectin-negative CCR7− effector and memory CD8(+) T cells enter reactive lymph nodes and kill dendritic cells. Nat Immunol 2007; 8: 743–752
  • Sallusto F, Mackay CR. Chemoattractants and their receptors in homeostasis and inflammation. Curr Opin Immunol 2004; 16: 724–731
  • Martin-Fontecha A, Thomsen LL, Brett S, Gerard C, Lipp M, Lanzavecchia A, Sallusto F. Induced recruitment of NK cells to lymph nodes provides IFN-y for TH 1 priming. Nat Immunol 2004; 5(12)1260–1265
  • McEvoy LM, Jutila MA, Tsao PS, Cooke JP, Butcher EC. Anti-CD43 inhibits monocyte-endothelial adhesion in inflammation and atherogenesis. Blood 1997; 90: 3587–3594
  • Janatpour MJ, Hudak S, Sathe M, Sedgwick JD, McEvoy LM. Tumor necrosis factor-dependent segmental control of MIG expression by high endothelial venules in inflamed lymph nodes regulates monocyte recruitment. J Exp Med 2001; 194: 1375–1384
  • Hasday JD, Bannerman D, Sakarya S, Cross AS, Singh IS, Howard D, Drysdale BE, Goldblum SE. Exposure to febrile temperature modifies endothelial cell response to tumor necrosis factor-alpha. J Appl Physiol 2001; 90: 90–98
  • Shah A, Unger E, Bain MD, Bruce R, Bodkin J, Ginnetti J, Wang WC, Seon B, Stewart CC, Evans SS. Cytokine and adhesion molecule expression in primary human endothelial cells stimulated with fever-range hyperthermia. Int J Hyperthermia 2002; 18: 534–551
  • Lefor AT, Foster III CE, Sartor W, Engbrecht B, Fabian DF, Silverman D. Hyperthermia increases intercellular adhesion molecule-1 expression and lymphocyte adhesion to endothelial cells. Surgery 1994; 116: 214–220
  • Gnant MF, Turner EM, Alexander Jr HR. Effects of hyperthermia and tumour necrosis factor on inflammatory cytokine secretion and procoagulant activity in endothelial cells. Cytokine 2000; 12: 339–347
  • Nakayama J, Terao H, Koga T, Furue M. Induction of CD54 and CD58 Expression in cultured human endothelial cells by beta-interferon with or without hyperthermia in vitro. J Dermatol Sci 2001; 26: 19–24
  • Ito A, Shinkai M, Honda H, Wakabayashi T, Yoshida J, Kobayashi T. Augmentation of MHC class I antigen presentation via heat shock protein expression by hyperthermia. Cancer Immunol Immunother 2001; 50: 515–522
  • Nakabe N, Kokura S, Shimozawa M, Katada K, Sakamoto N, Ishikawa T, Handa O, Takagi T, Naito Y, Yoshida N, Yoshikawa T. Hyperthermia attenuates TNF-alpha-induced up regulation of endothelial cell adhesion molecules in human arterial endothelial cells. Int J Hyperthermia 2007; 23: 217–224
  • Frossard JL, Pastor CM, Hadengue A. Effect of hyperthermia on NF-κB binding activity in cerulein-induced acute pancreatitis. Am J Physiol Gastrointest Liver Physiol 2001; 280: G1157–1162
  • Jones SA. Directing transition from innate to acquired immunity: Defining a role for IL-6. J Immunol 2005; 175: 3463–3468
  • Rose-John S, Scheller J, Elson G, Jones SA. Interleukin-6 biology is coordinated by membrane-bound and soluble receptors: Role in inflammation and cancer. J Leukoc Biol 2006; 80: 227–236
  • Ostberg JR, Ertel BR, Lanphere JA. An important role for granulocytes in the thermal regulation of colon tumor growth. Immunol Invest 2005; 34: 259–272
  • Lin WW, Karin M. A cytokine-mediated link between innate immunity, inflammation, and cancer. J Clin Invest 2007; 117: 1175–1183
  • Coussens LM, Werb Z. Inflammation and cancer. Nature 2002; 420: 860–867
  • Balkwill F, Charles KA, Mantovani A. Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell 2005; 7: 211–217
  • Szlosarek P, Charles KA, Balkwill FR. Tumour necrosis factor-alpha as a tumour promoter. Eur J Cancer 2006; 42: 745–750
  • Becker C, Fantini MC, Schramm C, Lehr HA, Wirtz S, Nikolaev A, Burg J, Strand S, Kiesslich R, Huber S, et al. TGF-beta suppresses tumor progression in colon cancer by inhibition of IL-6 trans-signaling. Immunity 2004; 21: 491–501
  • Mitsuyama K, Sata M, Rose-John S. Interleukin-6 trans-signaling in inflammatory bowel disease. Cytokine Growth Factor Rev 2006; 17: 451–461
  • Atreya R, Neurath MF. Involvement of IL-6 in the pathogenesis of inflammatory bowel disease and colon cancer. Clin Rev Allergy Immunol 2005; 28: 187–196

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