Generation of MHC class i diversity in primary tumors and selection of the malignant phenotype

International Journal of Cancer

Volumn 138, Issue 2, 2016, Pages 271-280

  Garrido, Federico ^a,b,c   Romero, Irene ^a,b   Aptsiauri, Natalia ^a,b   Garcia Lora, Angel M ^a,b  

^a HOSPITAL UNIVERSITARIO VIRGEN DE LAS NIEVES   (Spain)

^b IBS Instituto de Investigación Biosanitaria de Granada   (Spain)

^c UNIVERSITY OF GRANADA   (Spain)

Author keywords

immune selection; immunoescape; intratumor heterogeneity; metastasis; MHC

Indexed keywords

HLA ANTIGEN CLASS 1;

ANIMAL; GENETICS; HUMAN; IMMUNOLOGY; NEOPLASM; PATHOLOGY; PHENOTYPE; TUMOR ESCAPE;

ANIMALS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; NEOPLASMS; PHENOTYPE; TUMOR ESCAPE;

EID: 84955507226     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.29375     Document Type: Article

References (104)

1. Fisher R, Pusztai L, Swanton C,. Cancer heterogeneity: implications for targeted therapeutics. Br J Cancer 2013; 108: 479-85.
2. De Sousa EMF, Vermeulen L, Fessler E, et al., Cancer heterogeneity-a multifaceted view. EMBO Rep 2013; 14: 686-95.
3. Lindberg J, Klevebring D, Liu W, et al., Exome sequencing of prostate cancer supports the hypothesis of independent tumour origins. Eur Urol 2013; 63: 347-53.
4. Gerlinger M, Rowan AJ, Horswell S, et al., Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med 2012; 366: 883-92.
5. Garrido F, Cabrera T, Concha A, et al., Natural history of HLA expression during tumour development. Immunol Today 1993; 14: 491-9.
6. Marincola FM, Jaffee EM, Hicklin DJ, et al., Escape of human solid tumors from T-cell recognition: molecular mechanisms and functional significance. Adv Immunol 2000; 74: 181-273.
7. Boon T, van der Bruggen P,. Human tumor antigens recognized by T lymphocytes. J Exp Med 1996; 183: 725-9.
8. Ljunggren HG, Karre K,. In search of the "missing self": MHC molecules and NK cell recognition. Immunol Today 1990; 11: 237-44.
9. Garrido C, Paco L, Romero I, et al., MHC class I molecules act as tumor suppressor genes regulating the cell cycle gene expression, invasion and intrinsic tumorigenicity of melanoma cells. Carcinogenesis 2012; 33: 687-93.
10. Garrido F, Ruiz-Cabello F, Cabrera T, et al., Implications for immunosurveillance of altered HLA class I phenotypes in human tumours. Immunol Today 1997; 18: 89-95.
11. Khong HT, Restifo NP,. Natural selection of tumor variants in the generation of "tumor escape" phenotypes. Nat Immunol 2002; 3: 999-1005.
12. Challa-Malladi M, Lieu YK, Califano O, et al., Combined genetic inactivation of beta2-Microglobulin and CD58 reveals frequent escape from immune recognition in diffuse large B cell lymphoma. Cancer Cell 2011; 20: 728-40.
13. Garrido F, Cabrera T, Aptsiauri N,. "Hard" and "soft" lesions underlying the HLA class I alterations in cancer cells: implications for immunotherapy. Int J Cancer 2010; 127: 249-56.
14. Garrido F, Algarra I, Garcia-Lora AM,. The escape of cancer from T lymphocytes: immunoselection of MHC class I loss variants harboring structural-irreversible "hard" lesions. Cancer Immunol Immunother 2010; 59: 1601-6.
15. Carretero R, Wang E, Rodriguez AI, et al., Regression of melanoma metastases after immunotherapy is associated with activation of antigen presentation and interferon-mediated rejection genes. Int J Cancer 2012; 131: 387-95.
16. Garrido A, Perez M, Delgado C, et al., Influence of class I H-2 gene expression on local tumor growth. Description of a model obtained from clones derived from a solid BALB/c tumor. Exp Clin Immunogenet 1986; 3: 98-110.
17. Garrido ML, Perez M, Delgado C, et al., Immunogenicity of H-2 positive and H-2 negative clones of a mouse tumour, GR9. J Immunogenet 1986; 13: 159-67.
18. Perez M, Algarra I, Ljunggren HG, et al., A weakly tumorigenic phenotype with high MHC class-I expression is associated with high metastatic potential after surgical removal of the primary murine fibrosarcoma. Int J Cancer 1990; 46: 258-61.
19. Garcia-Lora A, Algarra I, Gaforio JJ, et al., Immunoselection by T lymphocytes generates repeated MHC class I-deficient metastatic tumor variants. Int J Cancer 2001; 91: 109-19.
20. Algarra I, Gaforio JJ, Garrido A, et al., Heterogeneity of MHC-class-I antigens in clones of methylcholanthrene-induced tumors. Implications for local growth and metastasis. Int J Cancer Suppl 1991; 6: 73-81.
21. Eisenbach L, Hollander N, Greenfeld L, et al., The differential expression of H-2K versus H-2D antigens, distinguishing high-metastatic from low-metastatic clones, is correlated with the immunogenic properties of the tumor cells. Int J Cancer 1984; 34: 567-73.
22. VandenDriessche T, Geldhof A, Bakkus M, et al., Metastasis of mouse T lymphoma cells is controlled by the level of major histocompatibility complex class I H-2Dk antigens. Int J Cancer 1994; 58: 217-25.
23. Katzav S, Segal S, Feldman M,. Metastatic capacity of cloned T10 sarcoma cells that differ in H-2 expression: inverse relationship to their immunogenic potency. J Natl Cancer Inst 1985; 75: 307-18.
24. Garcia-Lora A, Martinez M, Algarra I, et al., MHC class I-deficient metastatic tumor variants immunoselected by T lymphocytes originate from the coordinated downregulation of APM components. Int J Cancer 2003; 106: 521-7.
25. Romero JM, Jimenez P, Cabrera T, et al., Coordinated downregulation of the antigen presentation machinery and HLA class I/beta2-microglobulin complex is responsible for HLA-ABC loss in bladder cancer. Int J Cancer 2005; 113: 605-10.
26. Vitale M, Rezzani R, Rodella L, et al., HLA class I antigen and transporter associated with antigen processing (TAP1 and TAP2) down-regulation in high-grade primary breast carcinoma lesions. Cancer Res 1998; 58: 737-42.
27. Restifo NP, Esquivel F, Kawakami Y, et al., Identification of human cancers deficient in antigen processing. J Exp Med 1993; 177: 265-72.
28. Manning J, Indrova M, Lubyova B, et al., Induction of MHC class I molecule cell surface expression and epigenetic activation of antigen-processing machinery components in a murine model for human papilloma virus 16-associated tumours. Immunology 2008; 123: 218-27.
29. Setiadi AF, Omilusik K, David MD, et al., Epigenetic enhancement of antigen processing and presentation promotes immune recognition of tumors. Cancer Res 2008; 68: 9601-7.
30. Romero I, Martinez M, Garrido C, et al., The tumour suppressor Fhit positively regulates MHC class I expression on cancer cells. J Pathol 2012; 227: 367-79.
31. Jimenez P, Canton J, Collado A, et al., Chromosome loss is the most frequent mechanism contributing to HLA haplotype loss in human tumors. Int J Cancer 1999; 83: 91-7.
32. Maleno I, Romero JM, Cabrera T, et al., LOH at 6p21.3 region and HLA class I altered phenotypes in bladder carcinomas. Immunogenetics 2006; 58: 503-10.
33. Carretero R, Romero JM, Ruiz-Cabello F, et al., Analysis of HLA class I expression in progressing and regressing metastatic melanoma lesions after immunotherapy. Immunogenetics 2008; 60: 439-47.
34. Bernal M, Ruiz-Cabello F, Concha A, et al., Implication of the beta2-microglobulin gene in the generation of tumor escape phenotypes. Cancer Immunol Immunother 2012; 61: 1359-71.
35. Fidler IJ, Kripke ML,. Metastasis results from preexisting variant cells within a malignant tumor. Science 1977; 197: 893-5.
36. Kripke ML, Gruys E, Fidler IJ,. Metastatic heterogeneity of cells from an ultraviolet light-induced murine fibrosarcoma of recent origin. Cancer Res 1978; 38: 2962-7.
37. Algarra I, Ohlen C, Perez M, et al., NK sensitivity and lung clearance of MHC-class-I-deficient cells within a heterogeneous fibrosarcoma. Int J Cancer 1989; 44: 675-80.
38. Algarra I, Perez M, Gaforio JJ, et al., In vivo activation of NK cells induces inhibition of lung colonization of H-2 positive and H-2 negative fibrosarcoma tumor clones. Clin Exp Metastasis 1994; 12: 31-6.
39. Algarra I, Perez M, Hoglund P, et al., Generation and control of metastasis in experimental tumor systems: inhibition of experimental metastases by a tilorone analogue. Int J Cancer 1993; 54: 518-23.
40. Algarra I, Gonzalez A, Perez M, et al., Effect of in vivo activation of natural killer (NK) cells by a tilorone analogue on the survival of mice injected intravenously with different experimental murine tumours. Clin Exp Immunol 1996; 103: 499-505.
41. Sturmhofel K, Hammerling GJ,. Reconstitution of H-2 class I expression by gene transfection decreases susceptibility to natural killer cells of an EL4 class I loss variant. Eur J Immunol 1990; 20: 171-7.
42. Franksson L, George E, Powis S, et al., Tumorigenicity conferred to lymphoma mutant by major histocompatibility complex-encoded transporter gene. J Exp Med 1993; 177: 201-5.
43. Garrido C, Romero I, Berruguilla E, et al., Immunotherapy eradicates metastases with reversible defects in MHC class I expression. Cancer Immunol Immunother 2011; 60: 1257-68.
44. Haywood GR, McKhann CF,. Antigenic specificities on murine sarcoma cells. Reciprocal relationship between normal transplantation antigens (H-2) and tumor-specific immunogenicity. J Exp Med 1971; 133: 1171-87.
45. Katzav S, De Baetselier P, Tartakovsky B, et al., Alterations in major histocompatibility complex phenotypes of mouse cloned T10 sarcoma cells: association with shifts from nonmetastatic to metastatic cells. J Natl Cancer Inst 1983; 71: 317-24.
46. Garrido F, Cabrera T, Accola RS, et al., HLA and cancer. HLA: genetic diversity of HLA: Functional and medical implication. Proc Twelfth Int Workshop Conf 1997; 1: 445-58.
47. Lopez-Nevot MA, Esteban F, Ferron A, et al., HLA class I gene expression on human primary tumours and autologous metastases: demonstration of selective losses of HLA antigens on colorectal, gastric and laryngeal carcinomas. Br J Cancer 1989; 59: 221-6.
48. Vitale M, Pelusi G, Taroni B, et al., HLA class I antigen down-regulation in primary ovary carcinoma lesions: association with disease stage. Clin Cancer Res 2005; 11: 67-72.
49. Watson NF, Ramage JM, Madjd Z, 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.
50. Rolland P, Deen S, Scott I, et al., Human leukocyte antigen class I antigen expression is an independent prognostic factor in ovarian cancer. Clin Cancer Res 2007; 13: 3591-6.
51. Zia A, Schildberg FW, Funke I,. MHC class I negative phenotype of disseminated tumor cells in bone marrow is associated with poor survival in R0M0 breast cancer patients. Int J Cancer 2001; 93: 566-70.
52. Zhang X, Lin A, Zhang JG, et al., Alteration of HLA-F and HLA I antigen expression in the tumor is associated with survival in patients with esophageal squamous cell carcinoma. Int J Cancer 2013; 132: 82-9.
53. Domingo-Domenech J, Vidal SJ, Rodriguez-Bravo V, et al., Suppression of acquired docetaxel resistance in prostate cancer through depletion of notch- and hedgehog-dependent tumor-initiating cells. Cancer Cell 2012; 22: 373-88.
54. Landsberg J, Kohlmeyer J, Renn M, et al., Melanomas resist T-cell therapy through inflammation-induced reversible dedifferentiation. Nature 2012; 490: 412-6.
55. Anichini A, Mortarini R, Nonaka D, et al., Association of antigen-processing machinery and HLA antigen phenotype of melanoma cells with survival in American Joint Committee on Cancer stage III and IV melanoma patients. Cancer Res 2006; 66: 6405-11.
56. Ogino T, Shigyo H, Ishii H, et al., HLA class I antigen down-regulation in primary laryngeal squamous cell carcinoma lesions as a poor prognostic marker. Cancer Res 2006; 66: 9281-9.
57. Seliger B, Stoehr R, Handke D, et al., Association of HLA class I antigen abnormalities with disease progression and early recurrence in prostate cancer. Cancer Immunol Immunother 2009; 59: 529-40.
58. Yeung JT, Hamilton RL, Ohnishi K, et al., LOH in the HLA class I region at 6p21 is associated with shorter survival in newly diagnosed adult glioblastoma. Clin Cancer Res 2013; 19: 1816-26.
59. Albertsson PA, Basse PH, Hokland M, et al., NK cells and the tumour microenvironment: implications for NK-cell function and anti-tumour activity. Trends Immunol 2003; 24: 603-9.
60. Esendagli G, Bruderek K, Goldmann T, et al., Malignant and non-malignant lung tissue areas are differentially populated by natural killer cells and regulatory T cells in non-small cell lung cancer. Lung Cancer 2008; 59: 32-40.
61. Galon J, Costes A, Sanchez-Cabo F, et al., Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006; 313: 1960-4.
62. Vitale M, Cantoni C, Pietra G, et al., Effect of tumor cells and tumor microenvironment on NK-cell function. Eur J Immunol 2014; 44: 1582-92.
63. del Campo AB, Kyte JA, Carretero J, et al., Immune escape of cancer cells with beta2-microglobulin loss over the course of metastatic melanoma. Int J Cancer 2014; 134: 102-13.
64. Halama N, Michel S, Kloor M, et al., Localization and density of immune cells in the invasive margin of human colorectal cancer liver metastases are prognostic for response to chemotherapy. Cancer Res 2011; 71: 5670-7.
65. Kim MS, Kuppireddy SV, Sakamuri S, et al., Rapid characterization of candidate biomarkers for pancreatic cancer using cell microarrays (CMAs). J Proteome Res 2012; 11: 5556-63.
66. Turcotte S, Katz SC, Shia J, et al., Tumor MHC class I expression improves the prognostic value of T-cell density in resected colorectal liver metastases. Cancer Immunol Res 2014; 2: 530-7.
67. Bandoh N, Ogino T, Katayama A, et al., HLA class I antigen and transporter associated with antigen processing downregulation in metastatic lesions of head and neck squamous cell carcinoma as a marker of poor prognosis. Oncol Rep 2010; 23: 933-9.
68. Saio M, Teicher M, Campbell G, et al., Immunocytochemical demonstration of down regulation of HLA class-I molecule expression in human metastatic breast carcinoma. Clin Exp Metastasis 2004; 21: 243-9.
69. Yoshii M, Tanaka H, Ohira M, et al., Association of MHC class I expression and lymph node metastasis of gastric carcinoma. Hepatogastroenterology 2013; 60: 611-5.
70. Paschen A, Mendez RM, Jimenez P, et al., Complete loss of HLA class I antigen expression on melanoma cells: a result of successive mutational events. Int J Cancer 2003; 103: 759-67.
71. Maleno I, Aptsiauri N, Cabrera T, et al., Frequent loss of heterozygosity in the beta2-microglobulin region of chromosome 15 in primary human tumors. Immunogenetics 2011; 63: 65-71.
72. Mendez R, Serrano A, Jager E, et al., Analysis of HLA class I expression in different metastases from two melanoma patients undergoing peptide immunotherapy. Tissue Antigens 2001; 57: 508-19.
73. Cabrera T, Lara E, Romero JM, et al., HLA class I expression in metastatic melanoma correlates with tumor development during autologous vaccination. Cancer Immunol Immunother 2007; 56: 709-17.
74. Ryschich E, Notzel T, Hinz U, et al., Control of T-cell-mediated immune response by HLA class I in human pancreatic carcinoma. Clin Cancer Res 2005; 11: 498-504.
75. Leone P, Shin EC, Perosa F, et al., MHC class I antigen processing and presenting machinery: organization, function, and defects in tumor cells. J Natl Cancer Inst 2013; 105: 1172-87.
76. Koopman LA, Corver WE, van der Slik AR, et al., Multiple genetic alterations cause frequent and heterogeneous human histocompatibility leukocyte antigen class I loss in cervical cancer. J Exp Med 2000; 191: 961-76.
77. Aptsiauri N, Cabrera T, Garcia-Lora A, et al., MHC class I antigens and immune surveillance in transformed cells. Int Rev Cytol 2007; 256: 139-89.
78. Maleno I, Lopez-Nevot MA, Cabrera T, et al., Multiple mechanisms generate HLA class I altered phenotypes in laryngeal carcinomas: high frequency of HLA haplotype loss associated with loss of heterozygosity in chromosome region 6p21. Cancer Immunol Immunother 2002; 51: 389-96.
79. Maleno I, Lopez Nevot MA, Seliger B, et al., Low frequency of HLA haplotype loss associated with loss of heterozygocity in chromosome region 6p21 in clear renal cell carcinomas. Int J Cancer 2004; 109: 636-8.
80. Rhiem K, Klein A, Munch M, et al., Chromosomal region 15q21.1 is a frequent target of allelic imbalance in advanced breast carcinomas. Int J Cancer 2003; 106: 74-7.
81. Poetsch M, Kleist B,. Loss of heterozygosity at 15q21.3 correlates with occurrence of metastases in head and neck cancer. Mod Pathol 2006; 19: 1462-9.
82. Perez B, Benitez R, Fernandez MA, et al., A new beta 2 microglobulin mutation found in a melanoma tumor cell line. Tissue Antigens 1999; 53: 569-72.
83. Chang CC, Campoli M, Restifo NP, et al., Immune selection of hot-spot beta 2-microglobulin gene mutations, HLA-A2 allospecificity loss, and antigen-processing machinery component down-regulation in melanoma cells derived from recurrent metastases following immunotherapy. J Immunol 2005; 174: 1462-71.
84. Jimenez P, Cabrera T, Mendez R, et al., A nucleotide insertion in exon 4 is responsible for the absence of expression of an HLA-A∗0301 allele in a prostate carcinoma cell line. Immunogenetics 2001; 53: 606-10.
85. Serrano A, Brady CS, Jimenez P, et al., A mutation determining the loss of HLA-A2 antigen expression in a cervical carcinoma reveals novel splicing of human MHC class I classical transcripts in both tumoral and normal cells. Immunogenetics 2000; 51: 1047-52.
86. Chen HL, Gabrilovich D, Tampe R, et al., A functionally defective allele of TAP1 results in loss of MHC class I antigen presentation in a human lung cancer. Nat Genet 1996; 13: 210-3.
87. Seliger B, Ritz U, Abele R, et al., Immune escape of melanoma: first evidence of structural alterations in two distinct components of the MHC class I antigen processing pathway. Cancer Res 2001; 61: 8647-50.
88. Restifo NP, Marincola FM, Kawakami Y, et al., Loss of functional beta 2-microglobulin in metastatic melanomas from five patients receiving immunotherapy. J Natl Cancer Inst 1996; 88: 100-8.
89. van Esch EM, Tummers B, Baartmans V, et al., Alterations in classical and nonclassical HLA expression in recurrent and progressive HPV-induced usual vulvar intraepithelial neoplasia and implications for immunotherapy. Int J Cancer 2014; 135: 830-42.
90. Maleno I, Cabrera CM, Cabrera T, et al., Distribution of HLA class I altered phenotypes in colorectal carcinomas: high frequency of HLA haplotype loss associated with loss of heterozygosity in chromosome region 6p21. Immunogenetics 2004; 56: 244-53.
91. Paschen A, Arens N, Sucker A, et al., The coincidence of chromosome 15 aberrations and beta2-microglobulin gene mutations is causative for the total loss of human leukocyte antigen class I expression in melanoma. Clin Cancer Res 2006; 12: 3297-305.
92. Aptsiauri N, Garcia-Lora A, Garrido F,. "Hard" and "soft" loss of MHC class I expression in cancer cells. In:, Ress B, ed. Tumor immunology and immunotherapy. Oxford, UK: Oxford University Press, 2014: 63-78.
93. Benitez R, Godelaine D, Lopez-Nevot MA, et al., Mutations of the beta2-microglobulin gene result in a lack of HLA class I molecules on melanoma cells of two patients immunized with MAGE peptides. Tissue Antigens 1998; 52: 520-9.
94. Carretero R, Cabrera T, Gil H, et al., Bacillus Calmette-Guerin immunotherapy of bladder cancer induces selection of human leukocyte antigen class I-deficient tumor cells. Int J Cancer 2011; 129: 839-46.
95. Klippel ZK, Chou J, Towlerton AM, et al., Immune escape from NY-ESO-1-specific T-cell therapy via loss of heterozygosity in the MHC. Gene Ther 2014; 21: 337-42.
96. Sin JI, Park JB, Lee IH, et al., Intratumoral electroporation of IL-12 cDNA eradicates established melanomas by Trp2(180-188)-specific CD8+ CTLs in a perforin/granzyme-mediated and IFN-gamma-dependent manner: application of Trp2(180-188) peptides. Cancer Immunol Immunother 2012; 61: 1671-82.
97. Baines J, Celis E,. Immune-mediated tumor regression induced by CpG-containing oligodeoxynucleotides. Clin Cancer Res 2003; 9: 2693-700.
98. Reinis M, Simova J, Indrova M, et al., CpG oligodeoxynucleotides are effective in therapy of minimal residual tumour disease after chemotherapy or surgery in a murine model of MHC class I-deficient, HPV16-associated tumours. Int J Oncol 2007; 30: 1247-51.
99. Reinis M, Simova J, Bubenik J,. Inhibitory effects of unmethylated CpG oligodeoxynucleotides on MHC class I-deficient and -proficient HPV16-associated tumours. Int J Cancer 2006; 118: 1836-42.
100. Simova J, Pollakova V, Indrova M, et al., Immunotherapy augments the effect of 5-azacytidine on HPV16-associated tumours with different MHC class I-expression status. Br J Cancer 2011; 105: 1533-41.
101. Indrova M, Bieblova J, Jandlova T, et al., Chemotherapy, IL-12 gene therapy and combined adjuvant therapy of HPV 16-associated MHC class I-proficient and -deficient tumours. Int J Oncol 2006; 28: 253-9.
102. Del Campo AB, Carretero J, Munoz JA, et al., Adenovirus expressing beta2-microglobulin recovers HLA class I expression and antitumor immunity by increasing T-cell recognition. Cancer Gene Ther 2014; 21: 317-32.
103. Romero I, Garrido C, Algarra I, et al., T lymphocytes restrain spontaneous metastases in permanent dormancy. Cancer Res 2014; 74: 1958-68.
104. Garrido F, Algarra I,. MHC antigens and tumor escape from immune surveillance. Adv Cancer Res 2001; 83: 117-58.