Skip to main content
Erschienen in: International Journal of Hematology 4/2012

01.10.2012 | Original Article

Elevated serum granulysin and its clinical relevance in mature NK-cell neoplasms

verfasst von: Nodoka Sekiguchi, Naoko Asano, Toshiro Ito, Kayoko Momose, Masanobu Momose, Fumihiro Ishida

Erschienen in: International Journal of Hematology | Ausgabe 4/2012

Einloggen, um Zugang zu erhalten

Abstract

Mature natural killer (NK)-cell neoplasms include extranodal NK/T cell lymphoma, nasal type (ENKL), aggressive NK-cell leukemia (ANKL) and chronic lymphoproliferative disorders of NK cells (CLPD-NK). Granulysin, a cytolytic granule protein, is expressed in cytotoxic T cells and NK cells, and is found in the sera as well, and functions as a cytotoxic and proinflammatory protein. Cytolytic proteins, such as granzyme B and perforin, have been shown to play crucial pathophysiological roles in NK/T cell neoplasms and have also been utilized for diagnostic purposes. Granulysin in NK-cell proliferative disorders, however, has yet to be fully analyzed. To elucidate the clinical relevance of granulysin in mature NK-cell neoplasms, we measured serum granulysin and analyzed cytolytic molecules immunohistologically. The median concentrations of serum granulysin were 39.0, 2.85, 2.8 and 1.35 ng/ml in ANKL, ENKL, CLPD-NK and healthy subjects, respectively (P < 0.01). Serum granulysin was significantly elevated in patients with ANKL compared with the levels in ENKL (P = 0.006) and CLPD-NK (P = 0.037). Furthermore, serum granulysin was correlated with whole-blood EBV viral load in ENKL and ANKL (P = 0.005) and was significantly reduced after treatment. Different expression patterns of cytolytic granule proteins were observed among the mature NK-cell neoplasms. Granulysin is closely associated with the characteristics of NK-cell neoplasms and serum granulysin may serve as a novel biomarker for these disorders.
Literatur
1.
Zurück zum Zitat Suzuki R. Leukemia and lymphoma of natural killer cells. J Clin Exp Hematopathol. 2005;45:20. Suzuki R. Leukemia and lymphoma of natural killer cells. J Clin Exp Hematopathol. 2005;45:20.
2.
Zurück zum Zitat Ishida F, Kwong YL. Diagnosis and management of natural killer-cell malignancies. Expert Rev Hematol. 2010;3:593–602.PubMedCrossRef Ishida F, Kwong YL. Diagnosis and management of natural killer-cell malignancies. Expert Rev Hematol. 2010;3:593–602.PubMedCrossRef
3.
Zurück zum Zitat Rabbani GR, Phyliky RL, Tefferi A. A long-term study of patients with chronic natural killer cell lymphocytosis. Br J Haematol. 1999;106:960–6.PubMedCrossRef Rabbani GR, Phyliky RL, Tefferi A. A long-term study of patients with chronic natural killer cell lymphocytosis. Br J Haematol. 1999;106:960–6.PubMedCrossRef
4.
Zurück zum Zitat Tefferi A, Li CY, Witzig TE, Dhodapkar MV, Okuno SH, Phyliky RL. Chronic natural killer cell lymphocytosis: a descriptive clinical study. Blood. 1994;84:2721–5.PubMed Tefferi A, Li CY, Witzig TE, Dhodapkar MV, Okuno SH, Phyliky RL. Chronic natural killer cell lymphocytosis: a descriptive clinical study. Blood. 1994;84:2721–5.PubMed
5.
Zurück zum Zitat Asano N, Suzuki R, Kagami Y, Ishida F, Kitamura K, Fukutani H, Morishima Y, Takeuchi K, Nakamura S. Clinicopathologic and prognostic significance of cytotoxic molecule expression in nodal peripheral T-cell lymphoma, unspecified. Am J Surg Pathol. 2005;29:1284–93.PubMedCrossRef Asano N, Suzuki R, Kagami Y, Ishida F, Kitamura K, Fukutani H, Morishima Y, Takeuchi K, Nakamura S. Clinicopathologic and prognostic significance of cytotoxic molecule expression in nodal peripheral T-cell lymphoma, unspecified. Am J Surg Pathol. 2005;29:1284–93.PubMedCrossRef
6.
Zurück zum Zitat Wu X, Li P, Zhao J, Yang X, Wang F, Yang YQ, Fang F, Xu Y, Zhang H, Wang WY, Yi C. A clinical study of 115 patients with extranodal natural killer/T-cell lymphoma, nasal type. Clin Oncol (R Coll Radiol). 2008;20:619–25.CrossRef Wu X, Li P, Zhao J, Yang X, Wang F, Yang YQ, Fang F, Xu Y, Zhang H, Wang WY, Yi C. A clinical study of 115 patients with extranodal natural killer/T-cell lymphoma, nasal type. Clin Oncol (R Coll Radiol). 2008;20:619–25.CrossRef
7.
Zurück zum Zitat Schwartz EJ, Molina-Kirsch H, Zhao S, Marinelli RJ, Warnke RA, Natkunam Y. Immunohistochemical characterization of nasal-type extranodal NK/T-cell lymphoma using a tissue microarray: an analysis of 84 cases. Am J Clin Pathol. 2008;130:343–51.PubMedCrossRef Schwartz EJ, Molina-Kirsch H, Zhao S, Marinelli RJ, Warnke RA, Natkunam Y. Immunohistochemical characterization of nasal-type extranodal NK/T-cell lymphoma using a tissue microarray: an analysis of 84 cases. Am J Clin Pathol. 2008;130:343–51.PubMedCrossRef
8.
Zurück zum Zitat Ko YH, Ree HJ, Kim WS, Choi WH, Moon WS, Kim SW. Clinicopathologic and genotypic study of extranodal nasal-type natural killer/T-cell lymphoma and natural killer precursor lymphoma among Koreans. Cancer. 2000;89:2106–16.PubMedCrossRef Ko YH, Ree HJ, Kim WS, Choi WH, Moon WS, Kim SW. Clinicopathologic and genotypic study of extranodal nasal-type natural killer/T-cell lymphoma and natural killer precursor lymphoma among Koreans. Cancer. 2000;89:2106–16.PubMedCrossRef
9.
Zurück zum Zitat Takahashi E, Asano N, Li C, Tanaka T, Shimada K, Shimada S, Yoshino T, Kojima M, Hara K, Eimoto T, Nakamura S. Nodal T/NK-cell lymphoma of nasal type: a clinicopathological study of six cases. Histopathology. 2008;52:585–96.PubMedCrossRef Takahashi E, Asano N, Li C, Tanaka T, Shimada K, Shimada S, Yoshino T, Kojima M, Hara K, Eimoto T, Nakamura S. Nodal T/NK-cell lymphoma of nasal type: a clinicopathological study of six cases. Histopathology. 2008;52:585–96.PubMedCrossRef
10.
Zurück zum Zitat Takeshita M, Yamamoto M, Kikuchi M, Kimura N, Nakayama J, Uike N, Daimaru H, Sawada H, Okamura T. Angiodestruction and tissue necrosis of skin-involving CD56 + NK/T-cell lymphoma are influenced by expression of cell adhesion molecules and cytotoxic granule and apoptosis-related proteins. Am J Clin Pathol. 2000;113:201–11.PubMedCrossRef Takeshita M, Yamamoto M, Kikuchi M, Kimura N, Nakayama J, Uike N, Daimaru H, Sawada H, Okamura T. Angiodestruction and tissue necrosis of skin-involving CD56 + NK/T-cell lymphoma are influenced by expression of cell adhesion molecules and cytotoxic granule and apoptosis-related proteins. Am J Clin Pathol. 2000;113:201–11.PubMedCrossRef
11.
Zurück zum Zitat Krensky AM, Clayberger C. Biology and clinical relevance of granulysin. Tissue Antigens. 2009;73:193–8.PubMedCrossRef Krensky AM, Clayberger C. Biology and clinical relevance of granulysin. Tissue Antigens. 2009;73:193–8.PubMedCrossRef
12.
Zurück zum Zitat Chung WH, Hung SI, Yang JY, Su SC, Huang SP, Wei CY, Chin SW, Chiou CC, Chu SC, Ho HC, Yang CH, Lu CF, Wu JY, Liao YD, Chen YT. Granulysin is a key mediator for disseminated keratinocyte death in Stevens–Johnson syndrome and toxic epidermal necrolysis. Nat Med. 2008;14:1343–50.PubMedCrossRef Chung WH, Hung SI, Yang JY, Su SC, Huang SP, Wei CY, Chin SW, Chiou CC, Chu SC, Ho HC, Yang CH, Lu CF, Wu JY, Liao YD, Chen YT. Granulysin is a key mediator for disseminated keratinocyte death in Stevens–Johnson syndrome and toxic epidermal necrolysis. Nat Med. 2008;14:1343–50.PubMedCrossRef
13.
Zurück zum Zitat Nagasawa M, Kawamoto H, Tsuji Y, Mizutani S. Transient increase of serum granulysin in a stage IVs neuroblastoma patient during spontaneous regression: case report. Int J Hematol. 2005;82:456–7.PubMedCrossRef Nagasawa M, Kawamoto H, Tsuji Y, Mizutani S. Transient increase of serum granulysin in a stage IVs neuroblastoma patient during spontaneous regression: case report. Int J Hematol. 2005;82:456–7.PubMedCrossRef
14.
Zurück zum Zitat Saigusa S, Ichikura T, Tsujimoto H, Sugasawa H, Majima T, Kawarabayashi N, Chochi K, Ono S, Kinoshita M, Seki S, Ogawa K, Mochizuki H. Serum granulysin level as a novel prognostic marker in patients with gastric carcinoma. J Gastroenterol Hepatol. 2007;22:1322–7.PubMedCrossRef Saigusa S, Ichikura T, Tsujimoto H, Sugasawa H, Majima T, Kawarabayashi N, Chochi K, Ono S, Kinoshita M, Seki S, Ogawa K, Mochizuki H. Serum granulysin level as a novel prognostic marker in patients with gastric carcinoma. J Gastroenterol Hepatol. 2007;22:1322–7.PubMedCrossRef
15.
Zurück zum Zitat Nagasawa M, Isoda T, Itoh S, Kajiwara M, Morio T, Shimizu N, Ogawa K, Nagata K, Nakamura M, Mizutani S. Analysis of serum granulysin in patients with hematopoietic stem-cell transplantation: its usefulness as a marker of graft-versus-host reaction. Am J Hematol. 2006;81:340–8.PubMedCrossRef Nagasawa M, Isoda T, Itoh S, Kajiwara M, Morio T, Shimizu N, Ogawa K, Nagata K, Nakamura M, Mizutani S. Analysis of serum granulysin in patients with hematopoietic stem-cell transplantation: its usefulness as a marker of graft-versus-host reaction. Am J Hematol. 2006;81:340–8.PubMedCrossRef
16.
Zurück zum Zitat Sarwal MM, Jani A, Chang S, Huie P, Wang Z, Salvatierra O Jr, Clayberger C, Sibley R, Krensky AM, Pavlakis M. Granulysin expression is a marker for acute rejection and steroid resistance in human renal transplantation. Hum Immunol. 2001;62:21–31.PubMedCrossRef Sarwal MM, Jani A, Chang S, Huie P, Wang Z, Salvatierra O Jr, Clayberger C, Sibley R, Krensky AM, Pavlakis M. Granulysin expression is a marker for acute rejection and steroid resistance in human renal transplantation. Hum Immunol. 2001;62:21–31.PubMedCrossRef
17.
Zurück zum Zitat Nagasawa M, Ogawa K, Imashuku S, Mizutani S. Serum granulysin is elevated in patients with hemophagocytic lymphohistiocytosis. Int J Hematol. 2007;86:470–3.PubMedCrossRef Nagasawa M, Ogawa K, Imashuku S, Mizutani S. Serum granulysin is elevated in patients with hemophagocytic lymphohistiocytosis. Int J Hematol. 2007;86:470–3.PubMedCrossRef
18.
Zurück zum Zitat Nagasawa M, Ogawa K, Nagata K, Shimizu N. Serum granulysin as a possible biomarker of natural killer cell neoplasms. Br J Haematol. 2009;148:812–4.PubMedCrossRef Nagasawa M, Ogawa K, Nagata K, Shimizu N. Serum granulysin as a possible biomarker of natural killer cell neoplasms. Br J Haematol. 2009;148:812–4.PubMedCrossRef
19.
Zurück zum Zitat Chan JKC, Jaffe ES, Raffeld E, Ko YH. Aggressive NK-cell leukemia. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, et al., editors. WHO classification of tumours of haematopoietic and lymphoic tissues. Lyon: IARC; 2008. p. 276–7. Chan JKC, Jaffe ES, Raffeld E, Ko YH. Aggressive NK-cell leukemia. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, et al., editors. WHO classification of tumours of haematopoietic and lymphoic tissues. Lyon: IARC; 2008. p. 276–7.
20.
Zurück zum Zitat Chan JKC, Quintanilla-Martinez L, Ferry JA, Peh SC. Extranodal NK/T-cell lymphoma, nasal type. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, et al., editors. WHO classification of tumours of haematopoietic and lymphoic tissues. Lyon: IARC; 2008. p. 285–8. Chan JKC, Quintanilla-Martinez L, Ferry JA, Peh SC. Extranodal NK/T-cell lymphoma, nasal type. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, et al., editors. WHO classification of tumours of haematopoietic and lymphoic tissues. Lyon: IARC; 2008. p. 285–8.
21.
Zurück zum Zitat Villamor N, Morice WG, Chan AC, Foucar K. Chronic lymphoproliferative disorders of NK cells. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, et al., editors. WHO classification of tumours of haematopoietic and lymphoic tissues. Lyon: IARC; 2008. p. 274–5. Villamor N, Morice WG, Chan AC, Foucar K. Chronic lymphoproliferative disorders of NK cells. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, et al., editors. WHO classification of tumours of haematopoietic and lymphoic tissues. Lyon: IARC; 2008. p. 274–5.
22.
Zurück zum Zitat Ishida F, Ko YH, Kim WS, Suzumiya J, Isobe Y, Oshimi K, Nakamura S, Suzuki R. Aggressive natural killer cell leukemia: therapeutic potential of l-asparaginase and allogeneic hematopoietic stem cell transplantation. Cancer Sci. 2012;103:1079–83.PubMedCrossRef Ishida F, Ko YH, Kim WS, Suzumiya J, Isobe Y, Oshimi K, Nakamura S, Suzuki R. Aggressive natural killer cell leukemia: therapeutic potential of l-asparaginase and allogeneic hematopoietic stem cell transplantation. Cancer Sci. 2012;103:1079–83.PubMedCrossRef
23.
Zurück zum Zitat Ogawa K, Takamori Y, Suzuki K, Nagasawa M, Takano S, Kasahara Y, Nakamura Y, Kondo S, Sugamura K, Nakamura M, Nagata K. Granulysin in human serum as a marker of cell-mediated immunity. Eur J Immunol. 2003;33:1925–33.PubMedCrossRef Ogawa K, Takamori Y, Suzuki K, Nagasawa M, Takano S, Kasahara Y, Nakamura Y, Kondo S, Sugamura K, Nakamura M, Nagata K. Granulysin in human serum as a marker of cell-mediated immunity. Eur J Immunol. 2003;33:1925–33.PubMedCrossRef
24.
Zurück zum Zitat Ito T, Makishima H, Nakazawa H, Kobayashi H, Shimodaira S, Nakazawa Y, Kitano K, Matsuda K, Hidaka E, Ishida F. Promising approach for aggressive NK cell leukaemia with allogeneic haematopoietic cell transplantation. Eur J Haematol. 2008;81:107–11.PubMedCrossRef Ito T, Makishima H, Nakazawa H, Kobayashi H, Shimodaira S, Nakazawa Y, Kitano K, Matsuda K, Hidaka E, Ishida F. Promising approach for aggressive NK cell leukaemia with allogeneic haematopoietic cell transplantation. Eur J Haematol. 2008;81:107–11.PubMedCrossRef
25.
Zurück zum Zitat Makishima H, Ito T, Asano N, Nakazawa H, Shimodaira S, Kamijo Y, Nakazawa Y, Suzuki T, Kobayashi H, Kiyosawa K, Ishida F. Significance of chemokine receptor expression in aggressive NK cell leukemia. Leukemia. 2005;19:1169–74.PubMedCrossRef Makishima H, Ito T, Asano N, Nakazawa H, Shimodaira S, Kamijo Y, Nakazawa Y, Suzuki T, Kobayashi H, Kiyosawa K, Ishida F. Significance of chemokine receptor expression in aggressive NK cell leukemia. Leukemia. 2005;19:1169–74.PubMedCrossRef
26.
Zurück zum Zitat Makishima H, Ito T, Momose K, Nakazawa H, Shimodaira S, Kamijo Y, Nakazawa Y, Ichikawa N, Ueno M, Kobayashi H, Kitano K, Saito H, Kiyosawa K, Ishida F. Chemokine system and tissue infiltration in aggressive NK-cell leukemia. Leuk Res. 2007;31:1237–45.PubMedCrossRef Makishima H, Ito T, Momose K, Nakazawa H, Shimodaira S, Kamijo Y, Nakazawa Y, Ichikawa N, Ueno M, Kobayashi H, Kitano K, Saito H, Kiyosawa K, Ishida F. Chemokine system and tissue infiltration in aggressive NK-cell leukemia. Leuk Res. 2007;31:1237–45.PubMedCrossRef
27.
Zurück zum Zitat Ishida F, Nishina S, Asano N, Sasaki S, Sekiguchi N, Nakazawa H, Ito T, Shikama N. Late relapse of extranodal natural killer/T cell lymphoma, nasal type, after more than ten years. Leuk Lymphoma. 2010;51:171–3.PubMedCrossRef Ishida F, Nishina S, Asano N, Sasaki S, Sekiguchi N, Nakazawa H, Ito T, Shikama N. Late relapse of extranodal natural killer/T cell lymphoma, nasal type, after more than ten years. Leuk Lymphoma. 2010;51:171–3.PubMedCrossRef
28.
Zurück zum Zitat Suzuki R, Suzumiya J, Yamaguchi M, Nakamura S, Kameoka J, Kojima H, Abe M, Kinoshita T, Yoshino T, Iwatsuki K, Kagami Y, Tsuzuki T, Kurokawa M, Ito K, Kawa K, Oshimi K. Prognostic factors for mature natural killer (NK) cell neoplasms: aggressive NK cell leukemia and extranodal NK cell lymphoma, nasal type. Ann Oncol. 2010;21:1032–40.PubMedCrossRef Suzuki R, Suzumiya J, Yamaguchi M, Nakamura S, Kameoka J, Kojima H, Abe M, Kinoshita T, Yoshino T, Iwatsuki K, Kagami Y, Tsuzuki T, Kurokawa M, Ito K, Kawa K, Oshimi K. Prognostic factors for mature natural killer (NK) cell neoplasms: aggressive NK cell leukemia and extranodal NK cell lymphoma, nasal type. Ann Oncol. 2010;21:1032–40.PubMedCrossRef
29.
Zurück zum Zitat Gansert JL, Kiessler V, Engele M, Wittke F, Rollinghoff M, Krensky AM, Porcelli SA, Modlin RL, Stenger S. Human NKT cells express granulysin and exhibit antimycobacterial activity. J Immunol. 2003;170:3154–61.PubMed Gansert JL, Kiessler V, Engele M, Wittke F, Rollinghoff M, Krensky AM, Porcelli SA, Modlin RL, Stenger S. Human NKT cells express granulysin and exhibit antimycobacterial activity. J Immunol. 2003;170:3154–61.PubMed
31.
Zurück zum Zitat Kishi A, Takamori Y, Ogawa K, Takano S, Tomita S, Tanigawa M, Niman M, Kishida T, Fujita S. Differential expression of granulysin and perforin by NK cells in cancer patients and correlation of impaired granulysin expression with progression of cancer. Cancer Immunol Immunother. 2002;50:604–14.PubMedCrossRef Kishi A, Takamori Y, Ogawa K, Takano S, Tomita S, Tanigawa M, Niman M, Kishida T, Fujita S. Differential expression of granulysin and perforin by NK cells in cancer patients and correlation of impaired granulysin expression with progression of cancer. Cancer Immunol Immunother. 2002;50:604–14.PubMedCrossRef
32.
Zurück zum Zitat Yamaguchi M, Kwong YL, Kim WS, Maeda Y, Hashimoto C, Suh C, Izutsu K, Ishida F, Isobe Y, Sueoka E, Suzumiya J, Kodama T, Kimura H, Hyo R, Nakamura S, Oshimi K, Suzuki R. Phase II study of SMILE chemotherapy for newly diagnosed stage IV, relapsed, or refractory extranodal natural killer (NK)/T-cell lymphoma, nasal type: the NK-Cell Tumor Study Group study. J Clin Oncol. 2011;29:4410–6.PubMedCrossRef Yamaguchi M, Kwong YL, Kim WS, Maeda Y, Hashimoto C, Suh C, Izutsu K, Ishida F, Isobe Y, Sueoka E, Suzumiya J, Kodama T, Kimura H, Hyo R, Nakamura S, Oshimi K, Suzuki R. Phase II study of SMILE chemotherapy for newly diagnosed stage IV, relapsed, or refractory extranodal natural killer (NK)/T-cell lymphoma, nasal type: the NK-Cell Tumor Study Group study. J Clin Oncol. 2011;29:4410–6.PubMedCrossRef
33.
Zurück zum Zitat Yamaguchi M, Tobinai K, Oguchi M, Ishizuka N, Kobayashi Y, Isobe Y, Ishizawa K, Maseki N, Itoh K, Usui N, Wasada I, Kinoshita T, Ohshima K, Matsuno Y, Terauchi T, Nawano S, Ishikura S, Kagami Y, Hotta T, Oshimi K. Phase I/II study of concurrent chemoradiotherapy for localized nasal natural killer/T-cell lymphoma: Japan Clinical Oncology Group Study JCOG0211. J Clin Oncol. 2009;27:5594–600.PubMedCrossRef Yamaguchi M, Tobinai K, Oguchi M, Ishizuka N, Kobayashi Y, Isobe Y, Ishizawa K, Maseki N, Itoh K, Usui N, Wasada I, Kinoshita T, Ohshima K, Matsuno Y, Terauchi T, Nawano S, Ishikura S, Kagami Y, Hotta T, Oshimi K. Phase I/II study of concurrent chemoradiotherapy for localized nasal natural killer/T-cell lymphoma: Japan Clinical Oncology Group Study JCOG0211. J Clin Oncol. 2009;27:5594–600.PubMedCrossRef
34.
Zurück zum Zitat Gamen S, Hanson DA, Kaspar A, Naval J, Krensky AM, Anel A. Granulysin-induced apoptosis. I. Involvement of at least two distinct pathways. J Immunol. 1998;161:1758–64.PubMed Gamen S, Hanson DA, Kaspar A, Naval J, Krensky AM, Anel A. Granulysin-induced apoptosis. I. Involvement of at least two distinct pathways. J Immunol. 1998;161:1758–64.PubMed
35.
Zurück zum Zitat Tewary P, Yang D, de la Rosa G, Li Y, Finn MW, Krensky AM, Clayberger C, Oppenheim JJ. Granulysin activates antigen-presenting cells through TLR4 and acts as an immune alarmin. Blood. 2010;116:3465–74.PubMedCrossRef Tewary P, Yang D, de la Rosa G, Li Y, Finn MW, Krensky AM, Clayberger C, Oppenheim JJ. Granulysin activates antigen-presenting cells through TLR4 and acts as an immune alarmin. Blood. 2010;116:3465–74.PubMedCrossRef
36.
Zurück zum Zitat Nava VE, Jaffe ES. The pathology of NK-cell lymphomas and leukemias. Adv Anat Pathol. 2005;12:27–34.PubMedCrossRef Nava VE, Jaffe ES. The pathology of NK-cell lymphomas and leukemias. Adv Anat Pathol. 2005;12:27–34.PubMedCrossRef
37.
Zurück zum Zitat Ohshima K, Suzumiya J, Shimazaki K, Kato A, Tanaka T, Kanda M, Kikuchi M. Nasal T/NK cell lymphomas commonly express perforin and Fas ligand: important mediators of tissue damage. Histopathology. 1997;31:444–50.PubMedCrossRef Ohshima K, Suzumiya J, Shimazaki K, Kato A, Tanaka T, Kanda M, Kikuchi M. Nasal T/NK cell lymphomas commonly express perforin and Fas ligand: important mediators of tissue damage. Histopathology. 1997;31:444–50.PubMedCrossRef
38.
Zurück zum Zitat Li T, Zhang B, Ye Y, Yin H. Immunohistochemical and genetic analysis of Chinese nasal natural killer/T-cell lymphomas. Hum Pathol. 2006;37:54–60.PubMedCrossRef Li T, Zhang B, Ye Y, Yin H. Immunohistochemical and genetic analysis of Chinese nasal natural killer/T-cell lymphomas. Hum Pathol. 2006;37:54–60.PubMedCrossRef
39.
Zurück zum Zitat Teruya-Feldstein J, Jaffe ES, Burd PR, Kanegane H, Kingma DW, Wilson WH, Longo DL, Tosato G. The role of Mig, the monokine induced by interferon-gamma, and IP-10, the interferon-gamma-inducible protein-10, in tissue necrosis and vascular damage associated with Epstein-Barr virus-positive lymphoproliferative disease. Blood. 1997;90:4099–105.PubMed Teruya-Feldstein J, Jaffe ES, Burd PR, Kanegane H, Kingma DW, Wilson WH, Longo DL, Tosato G. The role of Mig, the monokine induced by interferon-gamma, and IP-10, the interferon-gamma-inducible protein-10, in tissue necrosis and vascular damage associated with Epstein-Barr virus-positive lymphoproliferative disease. Blood. 1997;90:4099–105.PubMed
Metadaten
Titel
Elevated serum granulysin and its clinical relevance in mature NK-cell neoplasms
verfasst von
Nodoka Sekiguchi
Naoko Asano
Toshiro Ito
Kayoko Momose
Masanobu Momose
Fumihiro Ishida
Publikationsdatum
01.10.2012
Verlag
Springer Japan
Erschienen in
International Journal of Hematology / Ausgabe 4/2012
Print ISSN: 0925-5710
Elektronische ISSN: 1865-3774
DOI
https://doi.org/10.1007/s12185-012-1159-x

Weitere Artikel der Ausgabe 4/2012

International Journal of Hematology 4/2012 Zur Ausgabe

Update Onkologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.