CTLA4 blockade elicits paraneoplastic neurological disease in a mouse model

Brain

Volumn 139, Issue 11, 2016, Pages 2923-2934

  Yshii, Lidia M ^a,b   Gebauer, Christina M ^a   Pignolet, Béatrice ^a,c   Mauré, Emilie ^a   Quériault, Clémence ^a   Pierau, Mandy ^d   Saito, Hiromitsu ^e   Suzuki, Noboru ^e   Brunner Weinzierl, Monika ^d   Bauer, Jan ^f   Liblau, Roland ^a  

^a UNIVERSITÉ PAUL SABATIER   (France)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c TOULOUSE UNIVERSITY HOSPITAL   (France)

^d UNIVERSITY HOSPITAL MAGDEBURG   (Germany)

^e MIE UNIVERSITY   (Japan)

^f Medical University of Vienna   (Austria)

Author keywords

CTLA4; immunotherapy; neuroinflammation; paraneoplastic neurological disorder; Purkinje cells

Indexed keywords

CRE RECOMBINASE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY CTLA4; UNCLASSIFIED DRUG; ANTIBODY; CD8 ANTIGEN; CTLA4 PROTEIN, MOUSE; GT(ROSA)26SOR NON-CODING RNA, MOUSE; GUANINE NUCLEOTIDE EXCHANGE FACTOR; INFLUENZA VIRUS HEMAGGLUTININ; NEUROPEPTIDE; PCP2 PROTEIN, MOUSE; TUMOR ANTIGEN; UNTRANSLATED RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTIGEN SPECIFICITY; ARTICLE; BREAST CANCER CELL LINE; CANCER TRANSPLANTATION; CD8+ T LYMPHOCYTE; CELL MIGRATION; CONTROLLED STUDY; IN VIVO STUDY; MOTOR ACTIVITY; MOUSE; NERVOUS SYSTEM INFLAMMATION; NEUROPATHOLOGY; NONHUMAN; PARANEOPLASTIC NEUROPATHY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURKINJE CELL; WEIGHT REDUCTION; ANIMAL; BAGG ALBINO MOUSE; BODY WEIGHT; BREAST TUMOR; CD4+ T LYMPHOCYTE; CEREBELLUM; COMPLICATION; DRUG EFFECTS; FEMALE; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; MOVEMENT DISORDERS; PARANEOPLASTIC SYNDROMES, NERVOUS SYSTEM; PATHOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE; TUMOR CELL LINE;

ANIMALS; ANTIBODIES; ANTIGENS, CD8; ANTIGENS, NEOPLASM; BODY WEIGHT; BREAST NEOPLASMS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CEREBELLUM; CTLA-4 ANTIGEN; FEMALE; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; MOTOR ACTIVITY; MOVEMENT DISORDERS; NEUROPEPTIDES; PARANEOPLASTIC SYNDROMES, NERVOUS SYSTEM; PURKINJE CELLS; RNA, UNTRANSLATED;

EID: 84994516305     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/aww225     Document Type: Article

References (44)

1. Aboul-Enein F, Hoftberger R, Buxhofer-Ausch V, Drlicek M, Lassmann H, Budka H, et al. Neocortical neurones may be targeted by immune attack in anti-Yo paraneoplastic syndrome. Neuropathol Appl Neurobiol 2008; 34: 248-52.
2. Albert ML, Austin LM, Darnell RB. Detection and treatment of activated T cells in the cerebrospinal fluid of patients with paraneoplastic cerebellar degeneration. Ann Neurol 2000; 47: 9-17.
3. Albert ML, Darnell JC, Bender A, Francisco LM, Bhardwaj N, Darnell RB. Tumor-specific killer cells in paraneoplastic cerebellar degeneration. Nat Med 1998; 4: 1321-4.
4. Albert ML, Darnell RB. Paraneoplastic neurological degenerations: keys to tumour immunity. Nat Rev Cancer 2004; 4: 36-44.
5. Allison JP. Checkpoints. Cell 2015; 162: 1202-5.
6. Aslakson CJ, Miller FR. Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor. Cancer Res 1992; 52: 1399-405.
7. Bauer J, Lassmann H. Neuropathological Techniques to investigate central nervous system sections in multiple sclerosis. Methods Mol Biol 2016; 1304: 211-29.
8. Bertrand A, Kostine M, Barnetche T, Truchetet ME, Schaeverbeke T. Immune related adverse events associated with anti-CTLA-4 antibodies: systematic review and meta-analysis. BMC Med 2015; 13: 211.
9. Bien CG, Vincent A, Barnett MH, Becker AJ, Blumcke I, Graus F, et al. Immunopathology of autoantibody-associated encephalitides: clues for pathogenesis. Brain 2012; 135 (Pt 5): 1622-38.
10. Dalmau J, Graus F, Villarejo A, Posner JB, Blumenthal D, Thiessen B, et al. Clinical analysis of anti-Ma2-associated encephalitis. Brain 2004; 127 (Pt 8): 1831-44.
11. Dalmau J, Rosenfeld MR. Paraneoplastic syndromes of the CNS. Lancet Neurol 2008; 7: 327-40.
12. Furneaux HM, Rosenblum MK, Dalmau J, Wong E, Woodruff P, Graus F, et al. Selective expression of Purkinje-cell antigens in tumor tissue from patients with paraneoplastic cerebellar degeneration. N Engl J Med 1990; 322: 1844-51.
13. Gozzard P, Woodhall M, Chapman C, Nibber A, Waters P, Vincent A, et al. Paraneoplastic neurologic disorders in small cell lung carcinoma: A prospective study. Neurology 2015; 85: 235-9.
14. Graus F, Saiz A, Dalmau J. Antibodies and neuronal autoimmune disorders of the CNS. J Neurol 2010; 257: 509-17.
15. Halle S, Keyser KA, Stahl FR, Busche A, Marquardt A, Zheng X, et al. In Vivo Killing Capacity of Cytotoxic T Cells Is Limited and Involves Dynamic Interactions and T Cell Cooperativity. Immunity 2016; 44: 233-45.
16. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010; 363: 711-23.
17. Ise W, Kohyama M, Nutsch KM, Lee HM, Suri A, Unanue ER, et al. CTLA-4 suppresses the pathogenicity of self antigen-specific T cells by cell-intrinsic and cell-extrinsic mechanisms. Nat Immunol 2010; 11: 129-35.
18. Iwama S, De Remigis A, Callahan MK, Slovin SF, Wolchok JD, Caturegli P. Pituitary expression of CTLA-4 mediates hypophysitis secondary to administration of CTLA-4 blocking antibody. Sci Transl Med 2014; 6: 230ra45.
19. Johnson DB, Sullivan RJ, Ott PA, Carlino MS, Khushalani NI, Ye F, et al. Ipilimumab therapy in patients with advanced Melanoma and preexisting autoimmune disorders. JAMA Oncol 2016; 2: 234-40.
20. Kirberg J, Baron A, Jakob S, Rolink A, Karjalainen K, von Boehmer H. Thymic selection of CD8 + single positive cells with a class II major histocompatibility complex-restricted receptor. J Exp Med 1994; 180: 25-34.
21. Kuehn HS, Ouyang W, Lo B, Deenick EK, Niemela JE, Avery DT, et al. Immune dysregulation in human subjects with heterozygous germline mutations in CTLA4. Science 2014; 345: 1623-7.
22. Kvistborg P, Philips D, Kelderman S, Hageman L, Ottensmeier C, Joseph-Pietras D, et al. Anti-CTLA-4 therapy broadens the melanoma-reactive CD8 + T cell response. Sci Transl Med 2014; 6: 254ra128.
23. Leach DR, Krummel MF, Allison JP. Enhancement of antitumor immunity by CTLA-4 blockade. Science 1996; 271: 1734-6.
24. Martin-Blondel G, Pignolet B, Tietz S, Yshii L, Gebauer C, Perinat T, et al. Migration of encephalitogenic CD8 T cells into the central nervous system is dependent on the alpha4beta1-integrin. Eur J Immunol 2015; 45: 3302-12.
25. Mason WP, Graus F, Lang B, Honnorat J, Delattre JY, Valldeoriola F, et al. Small-cell lung cancer, paraneoplastic cerebellar degeneration and the Lambert-Eaton myasthenic syndrome. Brain 1997; 120 (Pt 8): 1279-300.
26. McConnell MJ, Huang YH, Datwani A, Shatz CJ. H2-K(b) and H2-D(b) regulate cerebellar long-term depression and limit motor learning. Proc Natl Acad Sci USA 2009; 106: 6784-9.
27. Miyata M, Miyata H, Mikoshiba K, Ohama E. Development of Purkinje cells in humans: An immunohistochemical study using a monoclonal antibody against the inositol 1, 4, 5-triphosphate type 1 receptor (IP3R1). Acta Neuropathol 1999; 98: 226-32.
28. Morgan DJ, Liblau R, Scott B, Fleck S, McDevitt HO, Sarvetnick N, et al. CD8( +) T cell-mediated spontaneous diabetes in neonatal mice. J Immunol 1996; 157: 978-83.
29. Pellkofer H, Schubart AS, Hoftberger R, Schutze N, Pagany M, Schuller M, et al. Modelling paraneoplastic CNS disease: T-cells specific for the onconeuronal antigen PNMA1 mediate autoimmune encephalomyelitis in the rat. Brain 2004; 127 (Pt 8): 1822-30.
30. Pignolet BS, Gebauer CM, Liblau RS. Immunopathogenesis of paraneoplastic neurological syndromes associated with anti-Hu antibodies: A beneficial antitumor immune response going awry. Oncoimmunology 2013; 2: e27384.
31. Robert C, Thomas L, Bondarenko I, O'Day S, Weber J, Garbe C, et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med 2011; 364: 2517-26.
32. Roberts WK, Blachere NE, Frank MO, Dousmanis A, Ransohoff RM, Darnell RB. A destructive feedback loop mediated by CXCL10 in central nervous system inflammatory disease. Ann Neurol 2015; 78: 619-29.
33. Ruocco MG, Pilones KA, Kawashima N, Cammer M, Huang J, Babb JS, et al. Suppressing T cell motility induced by anti-CTLA-4 monotherapy improves antitumor effects. J Clin Invest 2012; 122: 3718-30.
34. Saito H, Tsumura H, Otake S, Nishida A, Furukawa T, Suzuki N. L7/ Pcp-2-specific expression of Cre recombinase using knock-in approach. Biochem Biophys Res Commun 2005; 331: 1216-21.
35. Santomasso BD, Roberts WK, Thomas A, Williams T, Blachere NE, Dudley ME, et al. A T-cell receptor associated with naturally occurring human tumor immunity. Proc Natl Acad Sci USA 2007; 104: 19073-8.
36. Saxena A, Bauer J, Scheikl T, Zappulla J, Audebert M, Desbois S, et al. Cutting edge: multiple sclerosis-like lesions induced by effector CD8 T cells recognizing a sequestered antigen on oligodendrocytes. J Immunol 2008; 181: 1617-21.
37. Schubert D, Bode C, Kenefeck R, Hou TZ, Wing JB, Kennedy A, et al. Autosomal dominant immune dysregulation syndrome in humans with CTLA4 mutations. Nat Med 2014; 20: 1410-16.
38. Simpson TR, Li F, Montalvo-Ortiz W, Sepulveda MA, Bergerhoff K, Arce F, et al. Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti-CTLA-4 therapy against melanoma. J Exp Med 2013; 210: 1695-710.
39. Steinman L. Conflicting consequences of immunity to cancer versus autoimmunity to neurons: insights from paraneoplastic disease. Eur J Immunol 2014; 44: 3201-5.
40. Tuzun E, Zhou L, Baehring JM, Bannykh S, Rosenfeld MR, Dalmau J. Evidence for antibody-mediated pathogenesis in anti-NMDAR encephalitis associated with ovarian teratoma. Acta Neuropathol 2009; 118: 737-43.
41. Van Allen EM, Miao D, Schilling B, Shukla SA, Blank C, Zimmer L, et al. Genomic correlates of response to CTLA-4 blockade in metastatic melanoma. Science 2015; 350: 207-11.
42. Waterhouse P, Penninger JM, Timms E, Wakeham A, Shahinian A, Lee KP, et al. Lymphoproliferative disorders with early lethality in mice deficient in Ctla-4. Science 1995; 270: 985-8.
43. Williams TJ, Benavides DR, Patrice KA, Dalmau JO, de Avila AL, Le DT, et al. Association of autoimmune encephalitis with combined immune checkpoint inhibitor treatment for Metastatic cancer. JAMA Neurol 2016; 73: 928-33. doi:10. 1001.
44. Wing K, Onishi Y, Prieto-Martin P, Yamaguchi T, Miyara M, Fehervari Z, et al. CTLA-4 control over Foxp3 + regulatory T cell function. Science 2008; 322: 271-5.