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Published in: BMC Cancer 1/2006

Open Access 01-12-2006 | Research article

High-resolution analysis of HLA class I alterations in colorectal cancer

Authors: Jan Willem F Dierssen, Noel FCC de Miranda, Arend Mulder, Marjo van Puijenbroek, Willem Verduyn, Frans HJ Claas, Cornelis JH van de Velde, Gert Jan Fleuren, Cees J Cornelisse, Willem E Corver, Hans Morreau

Published in: BMC Cancer | Issue 1/2006

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Abstract

Background

Previous studies indicate that alterations in Human Leukocyte Antigen (HLA) class I expression are frequent in colorectal tumors. This would suggest serious limitations for immunotherapy-based strategies involving T-cell recognition. Distinct patterns of HLA surface expression might conceal different immune escape mechanisms employed by the tumors and are worth further study.

Method

We applied four-color multiparameter flow cytometry (FCM), using a large panel of alloantigen-specific anti-HLA-A and -B monoclonal antibodies, to study membranous expression of individual HLA alleles in freshly isolated colorectal cancer cell suspensions from 21 patients.

Results

Alterations in HLA class I phenotype were observed in 8 (38%) of the 21 tumors and comprised loss of a single A or B alleles in 4 cases, and loss of all four A and B alleles in the other 4 cases. Seven of these 8 tumors were located on the right side of the colon, and those showing loss of both HLA-A and -B membranous expression were all of the MSI-H phenotype.

Conclusion

FCM allows the discrimination of complex phenotypes related to the expression of HLA class I. The different patterns of HLA class I expression might underlie different tumor behavior and influence the success rate of immunotherapy.
Appendix
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Literature
1.
go back to reference Van Der Bruggen P, Zhang Y, Chaux P, Stroobant V, Panichelli C, Schultz ES, Chapiro J, Van Den Eynde BJ, Brasseur F, Boon T: Tumor-specific shared antigenic peptides recognized by human T cells. Immunol Rev. 2002, 188: 51-64. 10.1034/j.1600-065X.2002.18806.x.CrossRefPubMed Van Der Bruggen P, Zhang Y, Chaux P, Stroobant V, Panichelli C, Schultz ES, Chapiro J, Van Den Eynde BJ, Brasseur F, Boon T: Tumor-specific shared antigenic peptides recognized by human T cells. Immunol Rev. 2002, 188: 51-64. 10.1034/j.1600-065X.2002.18806.x.CrossRefPubMed
2.
go back to reference Ionov Y, Peinado MA, Malkhosyan S, Shibata D, Perucho M: Ubiquitous somatic mutations in simple repeated sequences reveal a new mechanism for colonic carcinogenesis. Nature. 1993, 363: 558-561. 10.1038/363558a0.CrossRefPubMed Ionov Y, Peinado MA, Malkhosyan S, Shibata D, Perucho M: Ubiquitous somatic mutations in simple repeated sequences reveal a new mechanism for colonic carcinogenesis. Nature. 1993, 363: 558-561. 10.1038/363558a0.CrossRefPubMed
3.
go back to reference Thibodeau SN, Bren G, Schaid D: Microsatellite instability in cancer of the proximal colon. Science. 1993, 260: 816-819. 10.1126/science.8484122.CrossRefPubMed Thibodeau SN, Bren G, Schaid D: Microsatellite instability in cancer of the proximal colon. Science. 1993, 260: 816-819. 10.1126/science.8484122.CrossRefPubMed
4.
go back to reference Linnebacher M, Gebert J, Rudy W, Woerner S, Yuan YP, Bork P, von Knebel DM: Frameshift peptide-derived T-cell epitopes: a source of novel tumor- specific antigens. Int J Cancer. 2001, 93: 6-11. 10.1002/ijc.1298.CrossRefPubMed Linnebacher M, Gebert J, Rudy W, Woerner S, Yuan YP, Bork P, von Knebel DM: Frameshift peptide-derived T-cell epitopes: a source of novel tumor- specific antigens. Int J Cancer. 2001, 93: 6-11. 10.1002/ijc.1298.CrossRefPubMed
5.
go back to reference Ishikawa T, Fujita T, Suzuki Y, Okabe S, Yuasa Y, Iwai T, Kawakami Y: Tumor-specific immunological recognition of frameshift-mutated peptides in colon cancer with microsatellite instability. Cancer Res. 2003, 63: 5564-5572.PubMed Ishikawa T, Fujita T, Suzuki Y, Okabe S, Yuasa Y, Iwai T, Kawakami Y: Tumor-specific immunological recognition of frameshift-mutated peptides in colon cancer with microsatellite instability. Cancer Res. 2003, 63: 5564-5572.PubMed
6.
go back to reference Saeterdal I, Bjorheim J, Lislerud K, Gjertsen MK, Bukholm IK, Olsen OC, Nesland JM, Eriksen JA, Moller M, Lindblom A, Gaudernack G: Frameshift-mutation-derived peptides as tumor-specific antigens in inherited and spontaneous colorectal cancer. Proc Natl Acad Sci U S A. 2001, 98: 13255-13260. 10.1073/pnas.231326898.CrossRefPubMedPubMedCentral Saeterdal I, Bjorheim J, Lislerud K, Gjertsen MK, Bukholm IK, Olsen OC, Nesland JM, Eriksen JA, Moller M, Lindblom A, Gaudernack G: Frameshift-mutation-derived peptides as tumor-specific antigens in inherited and spontaneous colorectal cancer. Proc Natl Acad Sci U S A. 2001, 98: 13255-13260. 10.1073/pnas.231326898.CrossRefPubMedPubMedCentral
7.
go back to reference Townsend A, Bodmer H: Antigen recognition by class I-restricted T lymphocytes. Annu Rev Immunol. 1989, 7: 601-624.CrossRefPubMed Townsend A, Bodmer H: Antigen recognition by class I-restricted T lymphocytes. Annu Rev Immunol. 1989, 7: 601-624.CrossRefPubMed
8.
go back to reference Kaklamanis L, Gatter KC, Hill AB, Mortensen N, Harris AL, Krausa P, McMichael A, Bodmer JG, Bodmer WF: Loss of HLA class-I alleles, heavy chains and beta 2-microglobulin in colorectal cancer. Int J Cancer. 1992, 51: 379-385.CrossRefPubMed Kaklamanis L, Gatter KC, Hill AB, Mortensen N, Harris AL, Krausa P, McMichael A, Bodmer JG, Bodmer WF: Loss of HLA class-I alleles, heavy chains and beta 2-microglobulin in colorectal cancer. Int J Cancer. 1992, 51: 379-385.CrossRefPubMed
9.
go back to reference Cabrera T, Collado A, Fernandez MA, Ferron A, Sancho J, Ruiz-Cabello F, Garrido F: High frequency of altered HLA class I phenotypes in invasive colorectal carcinomas. Tissue Antigens. 1998, 52: 114-123.CrossRefPubMed Cabrera T, Collado A, Fernandez MA, Ferron A, Sancho J, Ruiz-Cabello F, Garrido F: High frequency of altered HLA class I phenotypes in invasive colorectal carcinomas. Tissue Antigens. 1998, 52: 114-123.CrossRefPubMed
10.
go back to reference Momburg F, Ziegler A, Harpprecht J, Moller P, Moldenhauer G, Hammerling GJ: Selective loss of HLA-A or HLA-B antigen expression in colon carcinoma. J Immunol. 1989, 142: 352-358.PubMed Momburg F, Ziegler A, Harpprecht J, Moller P, Moldenhauer G, Hammerling GJ: Selective loss of HLA-A or HLA-B antigen expression in colon carcinoma. J Immunol. 1989, 142: 352-358.PubMed
11.
go back to reference Leong AS: Pitfalls in diagnostic immunohistology. Adv Anat Pathol. 2004, 11: 86-93. 10.1097/00125480-200403000-00002.CrossRefPubMed Leong AS: Pitfalls in diagnostic immunohistology. Adv Anat Pathol. 2004, 11: 86-93. 10.1097/00125480-200403000-00002.CrossRefPubMed
12.
go back to reference Ljunggren HG, Karre K: Host resistance directed selectively against H-2-deficient lymphoma variants. Analysis of the mechanism. J Exp Med. 1985, 162: 1745-1759. 10.1084/jem.162.6.1745.CrossRefPubMed Ljunggren HG, Karre K: Host resistance directed selectively against H-2-deficient lymphoma variants. Analysis of the mechanism. J Exp Med. 1985, 162: 1745-1759. 10.1084/jem.162.6.1745.CrossRefPubMed
13.
go back to reference Long EO: Tumor cell recognition by natural killer cells. Semin Cancer Biol. 2002, 12: 57-61. 10.1006/scbi.2001.0398.CrossRefPubMed Long EO: Tumor cell recognition by natural killer cells. Semin Cancer Biol. 2002, 12: 57-61. 10.1006/scbi.2001.0398.CrossRefPubMed
14.
go back to reference Oudshoorn M, Doxiadis II, PM BL, Voorter CE, Verduyn W, Claas FH: Functional versus structural matching: can the CTLp test be replaced by HLA allele typing?. Hum Immunol. 2002, 63: 176-184. 10.1016/S0198-8859(01)00384-6.CrossRefPubMed Oudshoorn M, Doxiadis II, PM BL, Voorter CE, Verduyn W, Claas FH: Functional versus structural matching: can the CTLp test be replaced by HLA allele typing?. Hum Immunol. 2002, 63: 176-184. 10.1016/S0198-8859(01)00384-6.CrossRefPubMed
15.
go back to reference Mulder A, Kardol M, Regan J, Buelow R, Claas F: Reactivity of twenty-two cytotoxic human monoclonal HLA antibodies towards soluble HLA class I in an enzyme-linked immunosorbent assay (PRA-STAT). Hum Immunol. 1997, 56: 106-113. 10.1016/S0198-8859(97)00146-8.CrossRefPubMed Mulder A, Kardol M, Regan J, Buelow R, Claas F: Reactivity of twenty-two cytotoxic human monoclonal HLA antibodies towards soluble HLA class I in an enzyme-linked immunosorbent assay (PRA-STAT). Hum Immunol. 1997, 56: 106-113. 10.1016/S0198-8859(97)00146-8.CrossRefPubMed
16.
go back to reference Demanet C, Mulder A, Deneys V, Worsham MJ, Maes P, Claas FH, Ferrone S: Down-regulation of HLA-A and HLA-Bw6, but not HLA-Bw4, allospecificities in leukemic cells: an escape mechanism from CTL and NK attack?. Blood. 2004, 103: 3122-3130. 10.1182/blood-2003-07-2500.CrossRefPubMed Demanet C, Mulder A, Deneys V, Worsham MJ, Maes P, Claas FH, Ferrone S: Down-regulation of HLA-A and HLA-Bw6, but not HLA-Bw4, allospecificities in leukemic cells: an escape mechanism from CTL and NK attack?. Blood. 2004, 103: 3122-3130. 10.1182/blood-2003-07-2500.CrossRefPubMed
17.
go back to reference Koopman LA, Mulder A, Corver WE, Anholts JD, Giphart MJ, Claas FH, Fleuren GJ: HLA class I phenotype and genotype alterations in cervical carcinomas and derivative cell lines. Tissue Antigens. 1998, 51: 623-636.CrossRefPubMed Koopman LA, Mulder A, Corver WE, Anholts JD, Giphart MJ, Claas FH, Fleuren GJ: HLA class I phenotype and genotype alterations in cervical carcinomas and derivative cell lines. Tissue Antigens. 1998, 51: 623-636.CrossRefPubMed
18.
go back to reference Mulder A, Kardol M, Blom J, Jolley WB, Melief CJ, Bruning H: A human monoclonal antibody, produced following in vitro immunization, recognizing an epitope shared by HLA-A2 subtypes and HLA-A28. Tissue Antigens. 1993, 42: 27-34.CrossRefPubMed Mulder A, Kardol M, Blom J, Jolley WB, Melief CJ, Bruning H: A human monoclonal antibody, produced following in vitro immunization, recognizing an epitope shared by HLA-A2 subtypes and HLA-A28. Tissue Antigens. 1993, 42: 27-34.CrossRefPubMed
19.
go back to reference Mulder A, Kardol M, Blom J, Jolley WB, Melief CJ, Bruning JW: Characterization of two human monoclonal antibodies reactive with HLA-B12 and HLA-B60, respectively, raised by in vitro secondary immunization of peripheral blood lymphocytes. Hum Immunol. 1993, 36: 186-192. 10.1016/0198-8859(93)90124-J.CrossRefPubMed Mulder A, Kardol M, Blom J, Jolley WB, Melief CJ, Bruning JW: Characterization of two human monoclonal antibodies reactive with HLA-B12 and HLA-B60, respectively, raised by in vitro secondary immunization of peripheral blood lymphocytes. Hum Immunol. 1993, 36: 186-192. 10.1016/0198-8859(93)90124-J.CrossRefPubMed
20.
go back to reference Corver WE, Koopman LA, Mulder A, Cornelisse CJ, Fleuren GJ: Distinction between HLA class I-positive and -negative cervical tumor subpopulations by multiparameter DNA flow cytometry. Cytometry. 2000, 41: 73-80. 10.1002/1097-0320(20000901)41:1<73::AID-CYTO10>3.0.CO;2-5.CrossRefPubMed Corver WE, Koopman LA, Mulder A, Cornelisse CJ, Fleuren GJ: Distinction between HLA class I-positive and -negative cervical tumor subpopulations by multiparameter DNA flow cytometry. Cytometry. 2000, 41: 73-80. 10.1002/1097-0320(20000901)41:1<73::AID-CYTO10>3.0.CO;2-5.CrossRefPubMed
21.
go back to reference Stam NJ, Vroom TM, Peters PJ, Pastoors EB, Ploegh HL: HLA-A- and HLA-B-specific monoclonal antibodies reactive with free heavy chains in western blots, in formalin-fixed, paraffin-embedded tissue sections and in cryo-immuno-electron microscopy. Int Immunol. 1990, 2: 113-125.CrossRefPubMed Stam NJ, Vroom TM, Peters PJ, Pastoors EB, Ploegh HL: HLA-A- and HLA-B-specific monoclonal antibodies reactive with free heavy chains in western blots, in formalin-fixed, paraffin-embedded tissue sections and in cryo-immuno-electron microscopy. Int Immunol. 1990, 2: 113-125.CrossRefPubMed
22.
go back to reference Stam NJ, Spits H, Ploegh HL: Monoclonal antibodies raised against denatured HLA-B locus heavy chains permit biochemical characterization of certain HLA-C locus products. J Immunol. 1986, 137: 2299-2306.PubMed Stam NJ, Spits H, Ploegh HL: Monoclonal antibodies raised against denatured HLA-B locus heavy chains permit biochemical characterization of certain HLA-C locus products. J Immunol. 1986, 137: 2299-2306.PubMed
23.
go back to reference de Leeuw WJ, van Puijenbroek M, Merx R, Wijnen JT, Brocker-Vriends AH, Tops C, Vasen H, Cornelisse CJ, Morreau H: Bias in detection of instability of the (C)8 mononucleotide repeat of MSH6 in tumours from HNPCC patients. Oncogene. 2001, 20: 6241-6244. 10.1038/sj.onc.1204795.CrossRefPubMed de Leeuw WJ, van Puijenbroek M, Merx R, Wijnen JT, Brocker-Vriends AH, Tops C, Vasen H, Cornelisse CJ, Morreau H: Bias in detection of instability of the (C)8 mononucleotide repeat of MSH6 in tumours from HNPCC patients. Oncogene. 2001, 20: 6241-6244. 10.1038/sj.onc.1204795.CrossRefPubMed
24.
go back to reference Kloor M, Becker C, Benner A, Woerner SM, Gebert J, Ferrone S, Doeberitz MV: Immunoselective pressure and human leukocyte antigen class I antigen machinery defects in microsatellite unstable colorectal cancers. Cancer Research. 2005, 65: 6418-6424. 10.1158/0008-5472.CAN-05-0044.CrossRefPubMed Kloor M, Becker C, Benner A, Woerner SM, Gebert J, Ferrone S, Doeberitz MV: Immunoselective pressure and human leukocyte antigen class I antigen machinery defects in microsatellite unstable colorectal cancers. Cancer Research. 2005, 65: 6418-6424. 10.1158/0008-5472.CAN-05-0044.CrossRefPubMed
25.
go back to reference de Leeuw WJ, Dierssen J, Vasen HF, Wijnen JT, Kenter GG, Meijers-Heijboer H, Brocker-Vriends A, Stormorken A, Moller P, Menko F, Cornelisse CJ, Morreau H: Prediction of a mismatch repair gene defect by microsatellite instability and immunohistochemical analysis in endometrial tumours from HNPCC patients. J Pathol. 2000, 192: 328-335. 10.1002/1096-9896(2000)9999:9999<::AID-PATH701>3.0.CO;2-2.CrossRefPubMed de Leeuw WJ, Dierssen J, Vasen HF, Wijnen JT, Kenter GG, Meijers-Heijboer H, Brocker-Vriends A, Stormorken A, Moller P, Menko F, Cornelisse CJ, Morreau H: Prediction of a mismatch repair gene defect by microsatellite instability and immunohistochemical analysis in endometrial tumours from HNPCC patients. J Pathol. 2000, 192: 328-335. 10.1002/1096-9896(2000)9999:9999<::AID-PATH701>3.0.CO;2-2.CrossRefPubMed
26.
go back to reference Jass JR, Whitehall VL, Young J, Leggett BA: Emerging concepts in colorectal neoplasia. Gastroenterology. 2002, 123: 862-876. 10.1053/gast.2002.35392.CrossRefPubMed Jass JR, Whitehall VL, Young J, Leggett BA: Emerging concepts in colorectal neoplasia. Gastroenterology. 2002, 123: 862-876. 10.1053/gast.2002.35392.CrossRefPubMed
27.
go back to reference Menon AG, Morreau H, Tollenaar RA, Alphenaar E, van Puijenbroek M, Putter H, Janssen-Van Rhijn CM, Van De Velde CJ, Fleuren GJ, Kuppen PJ: Down-regulation of HLA-A expression correlates with a better prognosis in colorectal cancer patients. Lab Invest. 2002, 82: 1725-1733.CrossRefPubMed Menon AG, Morreau H, Tollenaar RA, Alphenaar E, van Puijenbroek M, Putter H, Janssen-Van Rhijn CM, Van De Velde CJ, Fleuren GJ, Kuppen PJ: Down-regulation of HLA-A expression correlates with a better prognosis in colorectal cancer patients. Lab Invest. 2002, 82: 1725-1733.CrossRefPubMed
28.
go back to reference Giorda E, Sibilio L, Martayan A, Moretti S, Venturo I, Mottolese M, Ferrara GB, Cappellacci S, Eibenschutz L, Catricala C, Grammatico P, Giacomini P: The antigen processing machinery of class I human leukocyte antigens: linked patterns of gene expression in neoplastic cells. Cancer Res. 2003, 63: 4119-4127.PubMed Giorda E, Sibilio L, Martayan A, Moretti S, Venturo I, Mottolese M, Ferrara GB, Cappellacci S, Eibenschutz L, Catricala C, Grammatico P, Giacomini P: The antigen processing machinery of class I human leukocyte antigens: linked patterns of gene expression in neoplastic cells. Cancer Res. 2003, 63: 4119-4127.PubMed
29.
go back to reference van den Elsen PJ, Holling TM, Kuipers HF, van der Stoep N: Transcriptional regulation of antigen presentation. Curr Opin Immunol. 2004, 16: 67-75. 10.1016/j.coi.2003.11.015.CrossRefPubMed van den Elsen PJ, Holling TM, Kuipers HF, van der Stoep N: Transcriptional regulation of antigen presentation. Curr Opin Immunol. 2004, 16: 67-75. 10.1016/j.coi.2003.11.015.CrossRefPubMed
30.
go back to reference Braud VM, Allan DS, McMichael AJ: Functions of nonclassical MHC and non-MHC-encoded class I molecules. Curr Opin Immunol. 1999, 11: 100-108. 10.1016/S0952-7915(99)80018-1.CrossRefPubMed Braud VM, Allan DS, McMichael AJ: Functions of nonclassical MHC and non-MHC-encoded class I molecules. Curr Opin Immunol. 1999, 11: 100-108. 10.1016/S0952-7915(99)80018-1.CrossRefPubMed
31.
go back to reference Cohen GB, Gandhi RT, Davis DM, Mandelboim O, Chen BK, Strominger JL, Baltimore D: The selective downregulation of class I major histocompatibility complex proteins by HIV-1 protects HIV-infected cells from NK cells. Immunity. 1999, 10: 661-671. 10.1016/S1074-7613(00)80065-5.CrossRefPubMed Cohen GB, Gandhi RT, Davis DM, Mandelboim O, Chen BK, Strominger JL, Baltimore D: The selective downregulation of class I major histocompatibility complex proteins by HIV-1 protects HIV-infected cells from NK cells. Immunity. 1999, 10: 661-671. 10.1016/S1074-7613(00)80065-5.CrossRefPubMed
32.
go back to reference Bicknell DC, Rowan A, Bodmer WF: Beta 2-microglobulin gene mutations: a study of established colorectal cell lines and fresh tumors. Proc Natl Acad Sci U S A. 1994, 91: 4751-4756. 10.1073/pnas.91.11.4751.CrossRefPubMedPubMedCentral Bicknell DC, Rowan A, Bodmer WF: Beta 2-microglobulin gene mutations: a study of established colorectal cell lines and fresh tumors. Proc Natl Acad Sci U S A. 1994, 91: 4751-4756. 10.1073/pnas.91.11.4751.CrossRefPubMedPubMedCentral
33.
go back to reference Browning M, Petronzelli F, Bicknell D, Krausa P, Rowan A, Tonks S, Murray N, Bodmer J, Bodmer W: Mechanisms of loss of HLA class I expression on colorectal tumor cells. Tissue Antigens. 1996, 47: 364-371.CrossRefPubMed Browning M, Petronzelli F, Bicknell D, Krausa P, Rowan A, Tonks S, Murray N, Bodmer J, Bodmer W: Mechanisms of loss of HLA class I expression on colorectal tumor cells. Tissue Antigens. 1996, 47: 364-371.CrossRefPubMed
34.
go back to reference Bicknell DC, Kaklamanis L, Hampson R, Bodmer WF, Karran P: Selection for beta 2-microglobulin mutation in mismatch repair-defective colorectal carcinomas. Curr Biol. 1996, 6: 1695-1697. 10.1016/S0960-9822(02)70795-1.CrossRefPubMed Bicknell DC, Kaklamanis L, Hampson R, Bodmer WF, Karran P: Selection for beta 2-microglobulin mutation in mismatch repair-defective colorectal carcinomas. Curr Biol. 1996, 6: 1695-1697. 10.1016/S0960-9822(02)70795-1.CrossRefPubMed
35.
go back to reference Cabrera CM, Jimenez P, Cabrera T, Esparza C, Ruiz-Cabello F, Garrido F: Total loss of MHC class I in colorectal tumors can be explained by two molecular pathways: beta2-microglobulin inactivation in MSI-positive tumors and LMP7/TAP2 downregulation in MSI-negative tumors. Tissue Antigens. 2003, 61: 211-219. 10.1034/j.1399-0039.2003.00020.x.CrossRefPubMed Cabrera CM, Jimenez P, Cabrera T, Esparza C, Ruiz-Cabello F, Garrido F: Total loss of MHC class I in colorectal tumors can be explained by two molecular pathways: beta2-microglobulin inactivation in MSI-positive tumors and LMP7/TAP2 downregulation in MSI-negative tumors. Tissue Antigens. 2003, 61: 211-219. 10.1034/j.1399-0039.2003.00020.x.CrossRefPubMed
36.
go back to reference Lothe RA, Peltomaki P, Meling GI, Aaltonen LA, Nystrom-Lahti M, Pylkkanen L, Heimdal K, Andersen TI, Moller P, Rognum TO: Genomic instability in colorectal cancer: relationship to clinicopathological variables and family history. Cancer Res. 1993, 53: 5849-5852.PubMed Lothe RA, Peltomaki P, Meling GI, Aaltonen LA, Nystrom-Lahti M, Pylkkanen L, Heimdal K, Andersen TI, Moller P, Rognum TO: Genomic instability in colorectal cancer: relationship to clinicopathological variables and family history. Cancer Res. 1993, 53: 5849-5852.PubMed
37.
go back to reference Wright CM, Dent OF, Barker M, Newland RC, Chapuis PH, Bokey EL, Young JP, Leggett BA, Jass JR, Macdonald GA: Prognostic significance of extensive microsatellite instability in sporadic clinicopathological stage C colorectal cancer. Br J Surg. 2000, 87: 1197-1202. 10.1046/j.1365-2168.2000.01508.x.CrossRefPubMed Wright CM, Dent OF, Barker M, Newland RC, Chapuis PH, Bokey EL, Young JP, Leggett BA, Jass JR, Macdonald GA: Prognostic significance of extensive microsatellite instability in sporadic clinicopathological stage C colorectal cancer. Br J Surg. 2000, 87: 1197-1202. 10.1046/j.1365-2168.2000.01508.x.CrossRefPubMed
38.
go back to reference Dolcetti R, Viel A, Doglioni C, Russo A, Guidoboni M, Capozzi E, Vecchiato N, Macri E, Fornasarig M, Boiocchi M: High prevalence of activated intraepithelial cytotoxic T lymphocytes and increased neoplastic cell apoptosis in colorectal carcinomas with microsatellite instability. Am J Pathol. 1999, 154: 1805-1813.CrossRefPubMedPubMedCentral Dolcetti R, Viel A, Doglioni C, Russo A, Guidoboni M, Capozzi E, Vecchiato N, Macri E, Fornasarig M, Boiocchi M: High prevalence of activated intraepithelial cytotoxic T lymphocytes and increased neoplastic cell apoptosis in colorectal carcinomas with microsatellite instability. Am J Pathol. 1999, 154: 1805-1813.CrossRefPubMedPubMedCentral
39.
go back to reference Jass JR, Do KA, Simms LA, Iino H, Wynter C, Pillay SP, Searle J, Radford-Smith G, Young J, Leggett B: Morphology of sporadic colorectal cancer with DNA replication errors. Gut. 1998, 42: 673-679.CrossRefPubMedPubMedCentral Jass JR, Do KA, Simms LA, Iino H, Wynter C, Pillay SP, Searle J, Radford-Smith G, Young J, Leggett B: Morphology of sporadic colorectal cancer with DNA replication errors. Gut. 1998, 42: 673-679.CrossRefPubMedPubMedCentral
40.
go back to reference Michael-Robinson JM, Biemer-Huttmann A, Purdie DM, Walsh MD, Simms LA, Biden KG, Young JP, Leggett BA, Jass JR, Radford-Smith GL: Tumour infiltrating lymphocytes and apoptosis are independent features in colorectal cancer stratified according to microsatellite instability status. Gut. 2001, 48: 360-366. 10.1136/gut.48.3.360.CrossRefPubMedPubMedCentral Michael-Robinson JM, Biemer-Huttmann A, Purdie DM, Walsh MD, Simms LA, Biden KG, Young JP, Leggett BA, Jass JR, Radford-Smith GL: Tumour infiltrating lymphocytes and apoptosis are independent features in colorectal cancer stratified according to microsatellite instability status. Gut. 2001, 48: 360-366. 10.1136/gut.48.3.360.CrossRefPubMedPubMedCentral
41.
go back to reference Young J, Simms LA, Biden KG, Wynter C, Whitehall V, Karamatic R, George J, Goldblatt J, Walpole I, Robin SA, Borten MM, Stitz R, Searle J, McKeone D, Fraser L, Purdie DR, Podger K, Price R, Buttenshaw R, Walsh MD, Barker M, Leggett BA, Jass JR: Features of colorectal cancers with high-level microsatellite instability occurring in familial and sporadic settings: parallel pathways of tumorigenesis. Am J Pathol. 2001, 159: 2107-2116.CrossRefPubMedPubMedCentral Young J, Simms LA, Biden KG, Wynter C, Whitehall V, Karamatic R, George J, Goldblatt J, Walpole I, Robin SA, Borten MM, Stitz R, Searle J, McKeone D, Fraser L, Purdie DR, Podger K, Price R, Buttenshaw R, Walsh MD, Barker M, Leggett BA, Jass JR: Features of colorectal cancers with high-level microsatellite instability occurring in familial and sporadic settings: parallel pathways of tumorigenesis. Am J Pathol. 2001, 159: 2107-2116.CrossRefPubMedPubMedCentral
42.
go back to reference Menon AG, Janssen-Van Rhijn CM, Morreau H, Putter H, Tollenaar RA, Van De Velde CJ, Fleuren GJ, Kuppen PJ: Immune system and prognosis in colorectal cancer: a detailed immunohistochemical analysis. Lab Invest. 2004, 84: 493-501. 10.1038/labinvest.3700055.CrossRefPubMed Menon AG, Janssen-Van Rhijn CM, Morreau H, Putter H, Tollenaar RA, Van De Velde CJ, Fleuren GJ, Kuppen PJ: Immune system and prognosis in colorectal cancer: a detailed immunohistochemical analysis. Lab Invest. 2004, 84: 493-501. 10.1038/labinvest.3700055.CrossRefPubMed
43.
go back to reference Gunderson LL, Sosin H: Areas of failure found at reoperation (second or symptomatic look) following "curative surgery" for adenocarcinoma of the rectum. Clinicopathologic correlation and implications for adjuvant therapy. Cancer. 1974, 34: 1278-1292. 10.1002/1097-0142(197410)34:4<1278::AID-CNCR2820340440>3.0.CO;2-F.CrossRefPubMed Gunderson LL, Sosin H: Areas of failure found at reoperation (second or symptomatic look) following "curative surgery" for adenocarcinoma of the rectum. Clinicopathologic correlation and implications for adjuvant therapy. Cancer. 1974, 34: 1278-1292. 10.1002/1097-0142(197410)34:4<1278::AID-CNCR2820340440>3.0.CO;2-F.CrossRefPubMed
Metadata
Title
High-resolution analysis of HLA class I alterations in colorectal cancer
Authors
Jan Willem F Dierssen
Noel FCC de Miranda
Arend Mulder
Marjo van Puijenbroek
Willem Verduyn
Frans HJ Claas
Cornelis JH van de Velde
Gert Jan Fleuren
Cees J Cornelisse
Willem E Corver
Hans Morreau
Publication date
01-12-2006
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2006
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/1471-2407-6-233

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