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Published in: World Journal of Surgical Oncology 1/2015

Open Access 01-12-2015 | Research

Prognostic value of HLA class I expression in patients with colorectal cancer

Authors: Yuji Iwayama, Tetsuhiro Tsuruma, Toru Mizuguchi, Tomohisa Furuhata, Nobuhiko Toyota, Masayuki Matsumura, Toshihiko Torigoe, Noriyuki Sato, Koichi Hirata

Published in: World Journal of Surgical Oncology | Issue 1/2015

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Abstract

Background

Prognostic factors are useful for determination of the therapeutic strategy and follow-up examination after curative operation in cancer treatment. The immunological state of the host can influence the prognosis for cancer patients as well as the features of the cancer. Human lymphocyte antigen (HLA) class I molecules have a central role in the anti-cancer immune system. Therefore, we focused on the HLA class I expression level in cancer cells to investigate its prognostic value in patients with colorectal cancer.

Methods

We reviewed the clinical pathology archives of 97 consecutive patients with stage II colorectal cancer who underwent curative operation at the Sapporo Medical University, Japan, from February 1994 to January 2005. Fifty-six high-risk patients had adjuvant chemotherapy. The cancer cell membrane immunoreactivity level for HLA class I expressed by EMR8-5 was classified into three categories (positive, dull, and negative). In this study, the cases were divided into two groups: “positive” and “dull/negative”. HLA class I expression level and clinicopathological parameters were evaluated with the Pearson χ 2 test. Survival analysis was assessed by the Kaplan-Meier methods, and the differences between survival curves were analyzed using the log-rank test.

Results

Immunohistochemical study of HLA class I revealed the following. There were 51 cases that were positive, 40 were dull, and six negative. The HLA class I expression level had no significant correlation with other clinicopathological parameters, except for gender. Univariate and multivariate analyses related to disease-free survival (DFS) revealed that tumor location, HLA expression level, and venous invasion were significant independent prognostic factors (P < 0.05). The 5-year DFS rates in HLA class I positive group and in the dull/negative group were 89% and 70%, respectively. For high-risk patients with adjuvant chemotherapy, the 5-year DFS rates in the HLA class I positive group and in the dull/negative group were 84% and 68%, respectively. For low-risk patients without the chemotherapy, the 5-year DFS rates in the HLA class I positive group and in the dull/negative group were 100% and 71%, respectively.

Conclusions

Our study concluded that the HLA class I expression level might be a very sensitive prognostic factor in colorectal cancer patients with stage II disease.
Literature
1.
go back to reference Weitz J, Koch M, Debus J, Hohler T, Galle PR, Buchler MW. Colorectal cancer. Lancet. 2005;365:153–65.CrossRefPubMed Weitz J, Koch M, Debus J, Hohler T, Galle PR, Buchler MW. Colorectal cancer. Lancet. 2005;365:153–65.CrossRefPubMed
2.
go back to reference Onogawa S, Kitadai Y, Tanaka S, Kuwai T, Kimura S, Chayama K. Expression of VEGF-C and VEGF-D at the invasive edge correlates with lymph node metastasis and prognosis of patients with colorectal carcinoma. Cancer Sci. 2004;95:32–9.CrossRefPubMed Onogawa S, Kitadai Y, Tanaka S, Kuwai T, Kimura S, Chayama K. Expression of VEGF-C and VEGF-D at the invasive edge correlates with lymph node metastasis and prognosis of patients with colorectal carcinoma. Cancer Sci. 2004;95:32–9.CrossRefPubMed
3.
go back to reference Wils J. Adjuvant treatment of colon cancer: past, present and future. J Chemotherapy. 2007;19:115–22.CrossRef Wils J. Adjuvant treatment of colon cancer: past, present and future. J Chemotherapy. 2007;19:115–22.CrossRef
4.
go back to reference Quasar Collaborative Group, Gray R, Barnwell J, McConkey C, Hills RK, Williams NS, et al. Adjuvant chemotherapy versus observation in patients with colorectal cancer: a randomized study. Lancet. 2007;370:2020–9.CrossRef Quasar Collaborative Group, Gray R, Barnwell J, McConkey C, Hills RK, Williams NS, et al. Adjuvant chemotherapy versus observation in patients with colorectal cancer: a randomized study. Lancet. 2007;370:2020–9.CrossRef
5.
go back to reference International Multicentre Pooled Analysis of B2 Colon Cancer Trials (IMPACT B2) Investigators. Efficacy of adjuvant fluorouracil and folinic acid in B2 colon cancer. J Clin Oncol. 1999;17:1356–63. International Multicentre Pooled Analysis of B2 Colon Cancer Trials (IMPACT B2) Investigators. Efficacy of adjuvant fluorouracil and folinic acid in B2 colon cancer. J Clin Oncol. 1999;17:1356–63.
6.
go back to reference O’Connor ES, Greenblatt DY, LoConte NK, Gangnon RE, Liou JI, Heise CP, et al. Adjuvant chemotherapy for stage II colon cancer with poor prognostic features. J Clin Oncol. 2011;29:3381–8.CrossRefPubMedCentralPubMed O’Connor ES, Greenblatt DY, LoConte NK, Gangnon RE, Liou JI, Heise CP, et al. Adjuvant chemotherapy for stage II colon cancer with poor prognostic features. J Clin Oncol. 2011;29:3381–8.CrossRefPubMedCentralPubMed
7.
go back to reference Wolpin BM, Meyerhardt JA, Mamon HJ, Mayer RJ. Adjuvant treatment of colorectal cancer. CA Cancer J Clin. 2007;57:168–85.CrossRefPubMed Wolpin BM, Meyerhardt JA, Mamon HJ, Mayer RJ. Adjuvant treatment of colorectal cancer. CA Cancer J Clin. 2007;57:168–85.CrossRefPubMed
8.
go back to reference Schmoll HJ, Van Cutsem E, Stein A, Valentini V, Glimelus B, Haustermans K, et al. ESMO Consensus Guidelines for management of patients with colon and rectal cancer. A personalized approach to clinical decision making. Ann Oncol. 2012;23:2479–516.CrossRefPubMed Schmoll HJ, Van Cutsem E, Stein A, Valentini V, Glimelus B, Haustermans K, et al. ESMO Consensus Guidelines for management of patients with colon and rectal cancer. A personalized approach to clinical decision making. Ann Oncol. 2012;23:2479–516.CrossRefPubMed
9.
go back to reference Marincola FM, Jaffee EM, Hicklin DJ, Ferrone S. Escape of human solid tumors from T-cell recognition: molecular mechanisms and functional significance. Adv Immunol. 2000;74:181–273.CrossRefPubMed Marincola FM, Jaffee EM, Hicklin DJ, Ferrone S. Escape of human solid tumors from T-cell recognition: molecular mechanisms and functional significance. Adv Immunol. 2000;74:181–273.CrossRefPubMed
10.
go back to reference Seliger B, Cabrera T, Garrido F, Ferrone S. HLA class I antigen abnormalities and immune escape by malignant cells. Semin Cancer Biol. 2002;12:3–13.CrossRefPubMed Seliger B, Cabrera T, Garrido F, Ferrone S. HLA class I antigen abnormalities and immune escape by malignant cells. Semin Cancer Biol. 2002;12:3–13.CrossRefPubMed
11.
go back to reference Raffaghello L, Prigione I, Airoldi I, Camoriano M, Morandi F, Bocca P, et al. Mechanisms of immune evasion of human neuroblastoma. Cancer Lett. 2005;228:155–61.CrossRefPubMed Raffaghello L, Prigione I, Airoldi I, Camoriano M, Morandi F, Bocca P, et al. Mechanisms of immune evasion of human neuroblastoma. Cancer Lett. 2005;228:155–61.CrossRefPubMed
12.
go back to reference Lopez-Albaitero A, Nayak JV, Ogino T, Machandia A, Gooding W, DeLeo AB, et al. Role of antigen-processing machinery in the in vitro resistance of squamous cell carcinoma of the head and neck cells to recognition by CTL. J Immunol. 2006;176:3402–9.CrossRefPubMed Lopez-Albaitero A, Nayak JV, Ogino T, Machandia A, Gooding W, DeLeo AB, et al. Role of antigen-processing machinery in the in vitro resistance of squamous cell carcinoma of the head and neck cells to recognition by CTL. J Immunol. 2006;176:3402–9.CrossRefPubMed
13.
go back to reference Torigoe T, Asanuma H, Nakazawa E, Tamura Y, Hirohashi Y, Yamamoto E, et al. Establishment of a monoclonal anti-pan HLA class I antibody suitable for immunostaining of formalin-fixed tissue: unusually high frequency of down-regulation in breast cancer tissues. Pathol Int. 2012;62:303–8.CrossRefPubMed Torigoe T, Asanuma H, Nakazawa E, Tamura Y, Hirohashi Y, Yamamoto E, et al. Establishment of a monoclonal anti-pan HLA class I antibody suitable for immunostaining of formalin-fixed tissue: unusually high frequency of down-regulation in breast cancer tissues. Pathol Int. 2012;62:303–8.CrossRefPubMed
14.
go back to reference Hata F, Sasaki K, Hirata K, Yamamitsu S, Shirasaka T. Efficacy of a continuous versus infusion of fluorouracil and daily divided dose cisplatin as adjuvant therapy in resectable colorectal cancer: a prospective randomized trial. Surg Today. 2008;38:623–32.CrossRefPubMed Hata F, Sasaki K, Hirata K, Yamamitsu S, Shirasaka T. Efficacy of a continuous versus infusion of fluorouracil and daily divided dose cisplatin as adjuvant therapy in resectable colorectal cancer: a prospective randomized trial. Surg Today. 2008;38:623–32.CrossRefPubMed
15.
go back to reference Tsukahara T, Kawaguchi S, Torigoe T, Asanuma H, Nakazawa E, Shimozawa K, et al. Prognostic significance of HLA class I expression in osteosarcoma defined by anti-pan HLA class I monoclonal antibody, EMR8-5. Cancer Sci. 2006;97:1374–80.CrossRefPubMed Tsukahara T, Kawaguchi S, Torigoe T, Asanuma H, Nakazawa E, Shimozawa K, et al. Prognostic significance of HLA class I expression in osteosarcoma defined by anti-pan HLA class I monoclonal antibody, EMR8-5. Cancer Sci. 2006;97:1374–80.CrossRefPubMed
16.
go back to reference Le Neel T, Moreau A, Laboisse C, Truchaud A. Comparative evaluation of automated systems in immunohistochemistry. Clin Chim Acta. 1998;278:185–92.CrossRefPubMed Le Neel T, Moreau A, Laboisse C, Truchaud A. Comparative evaluation of automated systems in immunohistochemistry. Clin Chim Acta. 1998;278:185–92.CrossRefPubMed
17.
go back to reference Kitamura H, Honma I, Torigoe T, Asanuma H, Sato N, Tsukamoto T. Down-regulation of HLA class I antigen is an independent prognostic factor for clear cell renal cell carcinoma. J Urol. 2007;177:1269–72.CrossRefPubMed Kitamura H, Honma I, Torigoe T, Asanuma H, Sato N, Tsukamoto T. Down-regulation of HLA class I antigen is an independent prognostic factor for clear cell renal cell carcinoma. J Urol. 2007;177:1269–72.CrossRefPubMed
18.
go back to reference Homma I, Kitamura H, Torigoe T, Tanaka T, Sato E, Hirohashi Y, et al. Human leukocyte antigen class I down-regulation in muscle-invasive bladder cancer: its association with clinical characteristics and survival after cystectomy. Cancer Sci. 2009;100:2331–4.CrossRefPubMed Homma I, Kitamura H, Torigoe T, Tanaka T, Sato E, Hirohashi Y, et al. Human leukocyte antigen class I down-regulation in muscle-invasive bladder cancer: its association with clinical characteristics and survival after cystectomy. Cancer Sci. 2009;100:2331–4.CrossRefPubMed
19.
go back to reference Kitamura H, Torigoe T, Honma I, Sato E, Asanuma H, Hirohashi Y, et al. Effects of human leukocyte antigen class I expression of tumor cells on outcome of intravesical instillation of bacillus Calmette-Guerin immunotherapy for bladder cancer. Clin Cancer Res. 2006;12:4641–4.CrossRefPubMed Kitamura H, Torigoe T, Honma I, Sato E, Asanuma H, Hirohashi Y, et al. Effects of human leukocyte antigen class I expression of tumor cells on outcome of intravesical instillation of bacillus Calmette-Guerin immunotherapy for bladder cancer. Clin Cancer Res. 2006;12:4641–4.CrossRefPubMed
20.
go back to reference Yabe H, Tsukahara T, Kawaguchi S, Wada T, Torigoe T, Sato N, et al. Prognostic significance of HLA class I expression in Ewing’s sarcoma family of tumors. J Surg Oncol. 2011;103:380–5.CrossRefPubMed Yabe H, Tsukahara T, Kawaguchi S, Wada T, Torigoe T, Sato N, et al. Prognostic significance of HLA class I expression in Ewing’s sarcoma family of tumors. J Surg Oncol. 2011;103:380–5.CrossRefPubMed
21.
go back to reference Madjd Z, Spendlove I, Pinder SE, Ellis IO, Durrant LG. Total loss of MHC class I is an independent indicator of good prognosis in breast cancer. Int J Cancer. 2005;117:248–55.CrossRefPubMed Madjd Z, Spendlove I, Pinder SE, Ellis IO, Durrant LG. Total loss of MHC class I is an independent indicator of good prognosis in breast cancer. Int J Cancer. 2005;117:248–55.CrossRefPubMed
22.
go back to reference Watson NF, Ramage JM, Madjd Z, Spendlove I, Ellis O, Scholefild JH, et al. Immunosurveillance is active in colorectal cancer as downregulation but not complete loss of MHC class I expression correlates with a poor prognosis. Int J Cancer. 2006;118:6–10.CrossRefPubMed Watson NF, Ramage JM, Madjd Z, Spendlove I, Ellis O, Scholefild JH, et al. Immunosurveillance is active in colorectal cancer as downregulation but not complete loss of MHC class I expression correlates with a poor prognosis. Int J Cancer. 2006;118:6–10.CrossRefPubMed
Metadata
Title
Prognostic value of HLA class I expression in patients with colorectal cancer
Authors
Yuji Iwayama
Tetsuhiro Tsuruma
Toru Mizuguchi
Tomohisa Furuhata
Nobuhiko Toyota
Masayuki Matsumura
Toshihiko Torigoe
Noriyuki Sato
Koichi Hirata
Publication date
01-12-2015
Publisher
BioMed Central
Published in
World Journal of Surgical Oncology / Issue 1/2015
Electronic ISSN: 1477-7819
DOI
https://doi.org/10.1186/s12957-015-0456-2

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