Microsatellite Instability: A Predictive Biomarker for Cancer Immunotherapy

Applied Immunohistochemistry and Molecular Morphology

Volumn 26, Issue 2, 2018, Pages e15-e21

  Chang, Liisa ^a   Chang, Minna ^b   Chang, Hanna M ^b   Chang, Fuju ^c,d  

^a MEDWAY NHS FOUNDATION TRUST   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d GUY'S AND ST THOMAS' NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

cancer treatment; immune checkpoint blockade; immunotherapy; microsatellite instability; mismatch repair; programmed cell death ligand 1; programmed cell death 1

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; FLUOROPYRIMIDINE; IRINOTECAN; OXALIPLATIN; PEMBROLIZUMAB; PROGRAMMED DEATH 1 RECEPTOR; PROSTATE SPECIFIC ANTIGEN; MONOCLONAL ANTIBODY; PHARMACOLOGICAL BIOMARKER; T LYMPHOCYTE RECEPTOR; TUMOR MARKER;

ARTICLE; BLADDER CANCER; CANCER IMMUNOTHERAPY; COLORECTAL CARCINOMA; DIGESTIVE SYSTEM CANCER; EPIGENETICS; FEMALE GENITAL TRACT CANCER; HEREDITARY NONPOLYPOSIS COLORECTAL CANCER; HODGKIN DISEASE; HUMAN; IMMUNOHISTOCHEMISTRY; MELANOMA; MICROSATELLITE INSTABILITY; MISMATCH REPAIR; NON SMALL CELL LUNG CANCER; POLYMERASE CHAIN REACTION; PREDICTIVE VALUE; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; PROSTATECTOMY; RENAL CELL CARCINOMA; SOMATIC MUTATION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR VOLUME; ANIMAL; DNA REPAIR; FOOD AND DRUG ADMINISTRATION; GENETICS; IMMUNOLOGY; IMMUNOTHERAPY; MUTATION; NEOPLASM; PROCEDURES; TREATMENT OUTCOME; UNITED STATES;

ANIMALS; ANTIBODIES, MONOCLONAL; BIOMARKERS, PHARMACOLOGICAL; BIOMARKERS, TUMOR; COSTIMULATORY AND INHIBITORY T-CELL RECEPTORS; DNA REPAIR; HUMANS; IMMUNOTHERAPY; MICROSATELLITE INSTABILITY; MUTATION; NEOPLASMS; TREATMENT OUTCOME; UNITED STATES; UNITED STATES FOOD AND DRUG ADMINISTRATION;

EID: 85043481224     PISSN: 15412016     EISSN: 15334058     Source Type: Journal    
DOI: 10.1097/PAI.0000000000000575     Document Type: Article

References (62)

1. Topalian SL, Hodi FS, Brahmer JR, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med. 2012; 366: 2443-2454.
2. Brahmer JR, Tykodi SS, Chow LQ, et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med. 2012; 366: 2455-2465.
3. Lipson EJ, Forde PM, Hammers HJ, et al. Antagonists of PD-1 and PD-L1 in cancer treatment. Semin Oncol. 2015; 42: 587-600.
4. Guan J, Lim KS, Mekhail T, et al. Programmed death ligand-1 (PDL1) expression in the programmed death receptor-1 (PD-1)/PD-L1 blockade: a key player against various cancers. Arch Pathol Lab Med. 2017; 141: 851-861.
5. Carbognin L, Pilotto S, Milella M, et al. Differential activity of nivolumab, pembrolizumab and MPDL3280A according to the tumor expression of programmed death-ligand-1 (PD-L1): sensitivity analysis of trials in melanoma, lung and genitourinary cancers. PLoS One. 2015; 10: e0130142.
6. Rizvi NA, Hellmann MD, Snyder A, et al. Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science. 2015; 348: 124-128.
7. Snyder A, Makarov V, Merghoub T, et al. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N Engl J Med. 2014; 371: 2189-2199.
8. Van Allen EM, Miao D, Schilling B, et al. Genomic correlates of response to CTLA-4 blockade in metastatic melanoma. Science. 2015; 350: 207-211.
9. Chalmers ZR, Connelly CF, Fabrizio D, et al. Analysis of 100, 000 human cancer genomes reveals the landscape of tumor mutational burden. Genome Med. 2017; 9: 34. Doi: 10. 1186/s13073-017-0424-2.
10. Jamieson NB, Maker AV. Gene-expression profiling to predict responsiveness to immunotherapy. Cancer Gene Ther. 2017; 24: 134-140.
11. Palmieri G, Colombino M, Cossu A, et al. Genetic instability and increased mutational load: which diagnostic tool best direct patients with cancer to immunotherapy? J Transl Med. 2017; 15: 17. Doi: 10. 1186/s12967-017-1119-6.
12. Le DT, Uram JN, Wang H, et al. PD-1 Blockade in tumors with mismatch-repair deficiency. N Engl J Med. 2015; 372: 2509-2520.
13. Dudley JC, Lin MT, Le DT, et al. Microsatellite instability as a biomarker for PD-1 blockade. Clin Cancer Res. 2016; 22: 813-820.
14. Naboush A, Roman CA, Shapira I. Immune checkpoint inhibitors in malignancies with mismatch repair deficiency: a review of the state of the current knowledge. J Investig Med. 2017; 65: 754-758.
15. Llosa NJ, Cruise M, Tam A, et al. The vigorous immune microenvironment of microsatellite instable colon cancer is balanced by multiple counter-inhibitory checkpoints. Cancer Discov. 2015; 5: 43-51.
16. FDA News Release. FDA approves first cancer treatment for any solid tumor with a specific genetic feature. 2017. Available at: www. fda. gov/NewsEvents/Newsroom/PressAnnouncements/ucm560167. htm. Accessed June 12, 2017.
17. Overman MJ, Lonardi S, Leone F, et al. Nivolumab in patients with DNA mismatch repair deficient/microsatellite instability high metastatic colorectal cancer: update from CheckMate 142. J Clin Oncol. 2017; 35 (4-suppl): 519-519.
18. Palomaki GE, McClain MR, Melillo S, et al. EGAPP supplementary evidence review: DNA testing strategies aimed at reducing morbidity and mortality from Lynch syndrome. Genet Med. 2009; 11: 42-65.
19. Shia J, Ellis NA, Klimstra DS. The utility of immunohistochemical detection of DNA mismatch repair gene proteins. Virchows Arch. 2004; 445: 431-441.
20. Shia J. Immunohistochemistry versus microsatellite instability testing for screening colorectal cancer patients at risk for hereditary nonpolyposis colorectal cancer syndrome. Part I. The utility of immunohistochemistry. J Mol Diagn. 2008; 10: 293-300.
21. Lynch HT, Synder CL, Shaw TG. Milestones of Lynch syndrome: 1895-2015. Nat Rev Cancer. 2015; 15: 181-194.
22. Boland CR, Goel A. Microsatellite instability in colorectal cancer. Gastroenterology. 2010; 138: 2073-2087.
23. Aarnio M, Sankila R, Pukkala E, et al. Cancer risk in mutation carriers of DNA-mismatch-repair genes. Int J Cancer. 1999; 81: 214-218.
24. Bansidhar BJ. Extracolonic manifestations of lynch syndrome. Clin Colon Rectal Surg. 2012; 25: 103-110.
25. Giardiello FM, Allen JI, Axilbund JE, et al. Guidelines on genetic evaluation and management of Lynch syndrome: a consensus statement by the US Multi-Society Task Force on Colorectal Cancer. Am J Gastroenterol. 2014; 109: 1159-1179.
26. Rosenbaum MW, Bledsoe JR, Morales-Oyarvide V, et al. PD-L1 expression in colorectal cancer is associated with microsatellite instability, BRAF mutation, medullary morphology and cytotoxic tumor-infiltrating lymphocytes. Mod Pathol. 2016; 29: 1104-1112.
27. Samowitz WS, Curtin K, Ma KN, et al. Microsatellite instability in sporadic colon cancer is associated with an improved prognosis at the population level. Cancer Epidemiol Biomarkers Prev. 2001; 10: 917-923.
28. Hampel H, Frankel WL, Martin E, et al. Screening for the Lynch syndrome (hereditary nonpolyposis colorectal cancer). N Engl J Med. 2005; 352: 1851-1860.
29. Bass AJ, Thorsson V, Shmulevich I, et al. Cancer Genome Atlas Research Network. Comprehensive molecular characterization of gastric adenocarcinoma. Nature. 2014; 513: 202-209.
30. Seo HM, Chang YS, Joo SH, et al. Clinicopathologic characteristics and outcomes of gastric cancers with the MSI-H phenotype. J Surg Oncol. 2009; 99: 143-147.
31. Farris AB III, Demicco EG, Le LP, et al. Clinicopathologic and molecular profiles of microsatellite unstable Barrett esophagusassociated adenocarcinoma. Am J Surg Pathol. 2011; 35: 647-655.
32. Ruemmele P, Dietmaier W, Terracciano L, et al. Histopathologic features and microsatellite instability of cancers of the papilla of vater and their precursor lesions. Am J Surg Pathol. 2009; 33: 691-704.
33. Laghi L, Beghelli S, Spinelli A, et al. Irrelevance of microsatellite instability in the epidemiology of sporadic pancreatic ductal adenocarcinoma. PLoS One. 2012; 7: e46002.
34. Nakata B, Wang YQ, Yashiro M, et al. Prognostic value of microsatellite instability in resectable pancreatic cancer. Clin Cancer Res. 2002; 8: 2536-2540.
35. Maple JT, Smyrk TC, Boardman LA, et al. Defective DNA mismatch repair in long-term (> or =3 years) survivors with pancreatic cancer. Pancreatology. 2005; 5: 220-228.
36. Chiappini F, Gross-Goupil M, Saffroy R, et al. Microsatellite instability mutator phenotype in hepatocellular carcinoma in nonalcoholic and non-virally infected normal livers. Carcinogenesis. 2004; 25: 541-547.
37. Hause RJ, Pritchard CC, Shendure J, et al. Classification and characterization of microsatellite instability across 18 cancer types. Nat Med. 2016; 22: 1342-1350.
38. Zighelboim I, Goodfellow PJ, Gao F, et al. Microsatellite instability and epigenetic inactivation of MLH1 and outcome of patients with endometrial carcinomas of the endometrioid type. J Clin Oncol. 2007; 25: 2042-2048.
39. Hampel H, Frankel W, Panescu J, et al. Screening for Lynch syndrome (hereditary nonpolyposis colorectal cancer) among endometrial cancer patients. Cancer Res. 2006; 66: 7810-7817.
40. Murphy MA, Wentzensen N. Frequency of mismatch repair deficiency in ovarian cancer: a systematic review. Int J Cancer. 2011; 129: 1914-1922.
41. Lazo PA. The molecular genetics of cervical carcinoma. Br J Cancer. 1999; 80: 2008-2018.
42. Cesinaro AM, Ubiali A, Sighinolfi P, et al. Mismatch repair proteins expression and microsatellite instability in skin lesions with sebaceous differentiation: a study in different clinical subgroups with and without extracutaneous cancer. Am J Dermatopathol. 2007; 29: 351-358.
43. Kruse R, Rutten A, Schweiger N, et al. Frequency of microsatellite instability in unselected sebaceous gland neoplasias and hyperplasias. J Invest Dermatol. 2003; 120: 858-864.
44. Palmieri G, Ascierto PA, Cossu A, et al. Assessment of genetic instability in melanocytic skin lesions through microsatellite analysis of benign naevi, dysplastic naevi, and primary melanomas and their metastases. Melanoma Res. 2003; 13: 167-170.
45. Kube?ek O, Kopecký J. Microsatellite instability in melanoma: a comprehensive review. Melanoma Res. 2016; 26: 545-550.
46. Mitmaker E, Alvarado C, Begin LR, et al. Microsatellite instability in benign and malignant thyroid neoplasms. J Surg Res. 2008; 150: 40-48.
47. Glavac D, Volavsek M, Potocnik U, et al. Low microsatellite instability and high loss of heterozygosity rates indicate dominant role of the suppressor pathway in squamous cell carcinoma of head and neck and loss of heterozygosity of 11q14. 3 correlates with tumor grade. Cancer Genet Cytogenet. 2003; 146: 27-32.
48. Hammerschmied C, Stoehr R, Walter B, et al. The role of elevated microsatellite alterations at selected tetranucleotides (EMAST) in renal cell carcinoma (RCC). Cancer Res. 2007; 67 (suppl): 1934.
49. Stoehr C, Burger M, Stoehr R, et al. Mismatch repair proteins hMLH1 and hMSH2 are differently expressed in the three main subtypes of sporadic renal cell carcinoma. Pathobiology. 2012; 79: 162-168.
50. Burger M, Denzinger S, Hammerschmied CG, et al. Elevated microsatellite alterations at selected tetranucleotides (EMAST) and mismatch repair gene expression in prostate cancer. J Mol Med (Berl). 2006; 84: 833-841.
51. Raymond VM, Mukherjee B, Wang F, et al. Elevated risk of prostate cancer among men with Lynch syndrome. J Clin Oncol. 2013; 31: 1713-1718.
52. Catto JW, Xinarianos G, Burton JL, et al. Differential expression of hMLH1 and hMSH2 is related to bladder cancer grade, stage and prognosis but not microsatellite instability. Int J Cancer. 2003; 105: 484-490.
53. Kawaguchi K, Oda Y, Takahira T, et al. Microsatellite instability and hMLH1 and hMSH2 expression analysis in soft tissue sarcomas. Oncol Rep. 2005; 13: 241-246.
54. Amant F, Dorfling CM, Dreyer L, et al. Microsatellite instability in uterine sarcomas. Int J Gynecol Cancer. 2001; 11: 218-223.
55. Saito T, Oda Y, Kawaguchi K, et al. Possible association between tumor-suppressor gene mutations and hMSH2/hMLH1 inactivation in alveolar soft part sarcoma. Hum Pathol. 2003; 34: 841-849.
56. Kazandjian D, Keegan P, Suzman DL, et al. Characterization of outcomes in patients with metastatic non-small cell lung cancer treated with programmed cell death protein 1 inhibitors past RECIST version 1. 1-defined disease progression in clinical trials. Semin Oncol. 2017; 44: 3-7.
57. Lote H, Cafferkey C, Chau I. PD-1 and PD-L1 blockade in gastrointestinal malignancies. Cancer Treat Rev. 2015; 41: 893-903.
58. Martin-Liberal J, Ochoa de Olza M, Hierro C, et al. The expanding role of immunotherapy. Cancer Treat Rev. 2017; 54: 74-86.
59. Moehler M, Delic M, Goepfert K, et al. Immunotherapy in gastrointestinal cancer: Recent results, current studies and future perspectives. Eur J Cancer. 2016; 59: 160-170.
60. Myint ZW, Goel G. Role of modern immunotherapy in gastrointestinal malignancies: a review of current clinical progress. J Hematol Oncol. 2017; 10: 86. Doi: 10. 1186/s13045-017-0454-7.
61. Carosella ED, Ploussard G, LeMaoult J, et al. A systematic review of immunotherapy in urologic cancer: evolving roles for targeting of CTLA-4, PD-1/PD-L1, and HLA-G. Eur Urol. 2015; 68: 267-279.
62. Heong V, Ngoi N, Tan DS. Update on immune checkpoint inhibitors in gynecological cancers. J Gynecol Oncol. 2017; 28: e20. Doi: 10. 3802/jgo. 2017. 28. e20.