Biochemical and immunologic effects of rituximab in patients with primary biliary cirrhosis and an incomplete response to ursodeoxycholic acid

Hepatology

Volumn 55, Issue 2, 2012, Pages 512-521

  Tsuda, Masanobu ^a,b   Moritoki, Yuki ^a,c   Lian, Zhe Xiong ^a,d   Zhang, Weici ^a   Yoshida, Katsunori ^a   Wakabayashi, Kanji ^a   Yang, Guo Xiang ^a   Nakatani, Toshio ^b   Vierling, John ^e   Lindor, Keith ^f   Gershwin, M Eric ^a   Bowlus, Christopher L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b KANSAI MEDICAL UNIVERSITY   (Japan)

^c AKITA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^e BAYLOR COLLEGE OF MEDICINE   (United States)

^f MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; MESSENGER RNA; METHYLPREDNISOLONE; MITOCHONDRION ANTIBODY; RITUXIMAB; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; URSODEOXYCHOLIC ACID;

ABDUCENS NERVE PARALYSIS; ADULT; ALKALINE PHOSPHATASE BLOOD LEVEL; ARTICLE; B LYMPHOCYTE; CD4+ CD25+ T LYMPHOCYTE; CELL FUNCTION; CELL STIMULATION; CLINICAL ARTICLE; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DRUG EFFICACY; DRUG SAFETY; DRY SKIN; FEMALE; HERPES ZOSTER; HUMAN; HYPERPIGMENTATION; IMMUNOGLOBULIN BLOOD LEVEL; LYMPHOCYTOPENIA; MEMORY CELL; OPEN STUDY; PRIMARY BILIARY CIRRHOSIS; PRIORITY JOURNAL; SINGLE DRUG DOSE; TREATMENT DURATION; TREATMENT RESPONSE; UNSPECIFIED SIDE EFFECT; UPPER RESPIRATORY TRACT INFECTION;

ADULT; ALKALINE PHOSPHATASE; ANTIBODIES, MONOCLONAL, MURINE-DERIVED; AUTOANTIBODIES; B-LYMPHOCYTES; CD4 LYMPHOCYTE COUNT; CHOLAGOGUES AND CHOLERETICS; FEMALE; HUMANS; IMMUNOLOGIC FACTORS; IMMUNOPHENOTYPING; LIVER; LIVER CIRRHOSIS, BILIARY; MIDDLE AGED; RNA, MESSENGER; T-LYMPHOCYTES; TREATMENT FAILURE; URSODEOXYCHOLIC ACID;

EID: 84863072278     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.24748     Document Type: Article

References (50)

1. Gershwin ME, Mackay IR. The causes of primary biliary cirrhosis: convenient and inconvenient truths. HEPATOLOGY 2008; 47: 737-745.
2. Kaplan MM, Gershwin ME. Primary biliary cirrhosis. N Engl J Med 2005; 353: 1261-1273.
3. Gershwin ME, Mackay IR, Sturgess A, Coppel RL. Identification and specificity of a cDNA encoding the 70 kd mitochondrial antigen recognized in primary biliary cirrhosis. J Immunol 1987; 138: 3525-3531.
4. Kamihira T, Shimoda S, Harada K, Kawano A, Handa M, Baba E, et al. Distinct costimulation dependent and independent autoreactive T-cell clones in primary biliary cirrhosis. Gastroenterology 2003; 125: 1379-1387.
5. Kita H, Matsumura S, He XS, Ansari AA, Lian ZX, Van de Water J, et al. Quantitative and functional analysis of PDC-E2-specific autoreactive cytotoxic T lymphocytes in primary biliary cirrhosis. J Clin Invest 2002; 109: 1231-1240.
6. Shimoda S, Ishikawa F, Kamihira T, Komori A, Niiro H, Baba E, et al. Autoreactive T-cell responses in primary biliary cirrhosis are proinflammatory whereas those of controls are regulatory. Gastroenterology 2006; 131: 606-618.
7. Lindgren S, Eriksson S. IgM in primary biliary cirrhosis. Physicochemical and complement activating properties. J Lab Clin Med 1982; 99: 636-645.
8. Kikuchi K, Lian ZX, Yang GX, Ansari AA, Ikehara S, Kaplan M, et al. Bacterial CpG induces hyper-IgM production in CD27(+) memory B cells in primary biliary cirrhosis. Gastroenterology 2005; 128: 304-312.
9. Moritoki Y, Lian ZX, Lindor K, Tuscano J, Tsuneyama K, Zhang W, et al. B-cell depletion with anti-CD20 ameliorates autoimmune cholangitis but exacerbates colitis in transforming growth factor-beta receptor II dominant negative mice. HEPATOLOGY 2009; 50: 1893-1903.
10. Lindor KD, Gershwin ME, Poupon R, Kaplan M, Bergasa NV, Heathcote EJ. Primary biliary cirrhosis. HEPATOLOGY 2009; 50: 291-308.
11. Pares A, Caballeria L, Rodes J. Excellent long-term survival in patients with primary biliary cirrhosis and biochemical response to ursodeoxycholic acid. Gastroenterology 2006; 130: 715-720.
12. Mitchison HC, Palmer JM, Bassendine MF, Watson AJ, Record CO, James OF. A controlled trial of prednisolone treatment in primary biliary cirrhosis. Three-year results. J Hepatol 1992; 15: 336-344.
13. Angulo P, Jorgensen RA, Keach JC, Dickson ER, Smith C, Lindor KD. Oral budesonide in the treatment of patients with primary biliary cirrhosis with a suboptimal response to ursodeoxycholic acid. HEPATOLOGY 2000; 31: 318-323.
14. Treiber G, Malfertheiner P. Mycophenolate mofetil for the treatment of primary biliary cirrhosis in patients with an incomplete response to ursodeoxycholic acid. J Clin Gastroenterol 2005; 39: 837-838; author reply 838.
15. Christensen E, Neuberger J, Crowe J, Altman DG, Popper H, Portmann B, et al. Beneficial effect of azathioprine and prediction of prognosis in primary biliary cirrhosis. Final results of an international trial. Gastroenterology 1985; 89: 1084-1091.
16. Minuk GY, Bohme CE, Burgess E, Hershfield NB, Kelly JK, Shaffer EA, et al. Pilot study of cyclosporin A in patients with symptomatic primary biliary cirrhosis. Gastroenterology 1988; 95: 1356-1363.
17. Reff ME, Carner K, Chambers KS, Chinn PC, Leonard JE, Raab R, et al. Depletion of B cells in vivo by a chimeric mouse human monoclonal antibody to CD20. Blood 1994; 83: 435-445.
18. Cohen SB, Emery P, Greenwald MW, Dougados M, Furie RA, Genovese MC, et al. Rituximab for rheumatoid arthritis refractory to anti-tumor necrosis factor therapy: Results of a multicenter, randomized, double-blind, placebo-controlled, phase III trial evaluating primary efficacy and safety at twenty-four weeks. Arthritis Rheum 2006; 54: 2793-2806.
19. Sanz I. Connective tissue diseases: The conundrum of B cell depletion in SLE. Nat Rev Rheumatol 2009; 5: 304-305.
20. Stasi R, Del Poeta G, Stipa E, Evangelista ML, Trawinska MM, Cooper N, et al. Response to B-cell depleting therapy with rituximab reverts the abnormalities of T-cell subsets in patients with idiopathic thrombocytopenic purpura. Blood 2007; 110: 2924-2930.
21. Stasi R, Pagano A, Stipa E, Amadori S. Rituximab chimeric anti-CD20 monoclonal antibody treatment for adults with chronic idiopathic thrombocytopenic purpura. Blood 2001; 98: 952-957.
22. Quartier P, Brethon B, Philippet P, Landman-Parker J, Le Deist F, Fischer A. Treatment of childhood autoimmune haemolytic anaemia with rituximab. Lancet 2001; 358: 1511-1513.
23. Eming R, Nagel A, Wolff-Franke S, Podstawa E, Debus D, Hertl M. Rituximab exerts a dual effect in pemphigus vulgaris. J Invest Dermatol 2008; 128: 2850-2858.
24. Dorner T, Isenberg D, Jayne D, Wiendl H, Zillikens D, Burmester G. Current status on B-cell depletion therapy in autoimmune diseases other than rheumatoid arthritis. Autoimmun Rev 2009; 9: 82-89.
25. Jacoby A, Rannard A, Buck D, Bhala N, Newton JL, James OF, et al. Development, validation, and evaluation of the PBC-40, a disease specific health related quality of life measure for primary biliary cirrhosis. Gut 2005; 54: 1622-1629.
26. Semple JW, Allen D, Chang W, Castaldi P, Freedman J. Rapid separation of CD4+ and CD19+ lymphocyte populations from human peripheral blood by a magnetic activated cell sorter (MACS). Cytometry 1993; 14: 955-960.
27. Sims GP, Ettinger R, Shirota Y, Yarboro CH, Illei GG, Lipsky PE. Identification and characterization of circulating human transitional B cells. Blood 2005; 105: 4390-4398.
28. Lan RY, Cheng C, Lian ZX, Tsuneyama K, Yang GX, Moritoki Y, et al. Liver-targeted and peripheral blood alterations of regulatory T cells in primary biliary cirrhosis. HEPATOLOGY 2006; 43: 729-737.
29. Corpechot C, Abenavoli L, Rabahi N, Chretien Y, Andreani T, Johanet C, et al. Biochemical response to ursodeoxycholic acid and long-term prognosis in primary biliary cirrhosis. HEPATOLOGY 2008; 48: 871-877.
30. Kuiper EM, Hansen BE, de Vries RA, den Ouden-Muller JW, van Ditzhuijsen TJ, Haagsma EB, et al. Improved prognosis of patients with primary biliary cirrhosis that have a biochemical response to ursodeoxycholic acid. Gastroenterology 2009; 136: 1281-1287.
31. Keogh KA, Wylam ME, Stone JH, Specks U. Induction of remission by B lymphocyte depletion in eleven patients with refractory antineutrophil cytoplasmic antibody-associated vasculitis. Arthritis Rheum 2005; 52: 262-268.
32. Pestronk A, Florence J, Miller T, Choksi R, Al-Lozi MT, Levine TD. Treatment of IgM antibody associated polyneuropathies using rituximab. J Neurol Neurosurg Psychiatry 2003; 74: 485-489.
33. Roll P, Palanichamy A, Kneitz C, Dorner T, Tony HP. Regeneration of B cell subsets after transient B cell depletion using anti-CD20 antibodies in rheumatoid arthritis. Arthritis Rheum 2006; 54: 2377-2386.
34. Vallerskog T, Gunnarsson I, Widhe M, Risselada A, Klareskog L, van Vollenhoven R, et al. Treatment with rituximab affects both the cellular and the humoral arm of the immune system in patients with SLE. Clin Immunol 2007; 122: 62-74.
35. Matsumura S, Van De Water J, Leung P, Odin JA, Yamamoto K, Gores GJ, et al. Caspase induction by IgA antimitochondrial antibody: IgA-mediated biliary injury in primary biliary cirrhosis. HEPATOLOGY 2004; 39: 1415-1422.
36. Lleo A, Bowlus CL, Yang GX, Invernizzi P, Podda M, Van de Water J, et al. Biliary apotopes and anti-mitochondrial antibodies activate innate immune responses in primary biliary cirrhosis. HEPATOLOGY 2010; 52: 987-998.
37. Leon MP, Spickett G, Jones DE, Bassendine MF. CD4+ T cell subsets defined by isoforms of CD45 in primary biliary cirrhosis. Clin Exp Immunol 1995; 99: 233-239.
38. Chuang YH, Lian ZX, Cheng CM, Lan RY, Yang GX, Moritoki Y, et al. Increased levels of chemokine receptor CXCR3 and chemokines IP-10 and MIG in patients with primary biliary cirrhosis and their first degree relatives. J Autoimmun 2005; 25: 126-132.
39. Shimoda S, Nakamura M, Ishibashi H, Hayashida K, Niho Y. HLA DRB4 0101-restricted immunodominant T cell autoepitope of pyruvate dehydrogenase complex in primary biliary cirrhosis: evidence of molecular mimicry in human autoimmune diseases. J Exp Med 1995; 181: 1835-1845.
40. Wakabayashi K, Lian ZX, Leung PS, Moritoki Y, Tsuneyama K, Kurth MJ, et al. Loss of tolerance in C57BL/6 mice to the autoantigen E2 subunit of pyruvate dehydrogenase by a xenobiotic with ensuing biliary ductular disease. HEPATOLOGY 2008; 48: 531-540.
41. Robinson AT, Miller N, Alexander DR. CD3 antigen-mediated calcium signals and protein kinase C activation are higher in CD45R0+ than in CD45RA+ human T lymphocyte subsets. Eur J Immunol 1993; 23: 61-68.
42. Iwata S, Saito K, Tokunaga M, Yamaoka K, Nawata M, Yukawa S, et al. Phenotypic changes of lymphocytes in patients with systemic lupus erythematosus who are in longterm remission after B cell depletion therapy with rituximab. J Rheumatol 2010;
43. Irie E, Shirota Y, Suzuki C, Tajima Y, Ishizawa K, Kameoka J, et al. Severe hypogammaglobulinemia persisting for 6 years after treatment with rituximab combined chemotherapy due to arrest of B lymphocyte differentiation together with alteration of T lymphocyte homeostasis. Int J Hematol 2010; 91: 501-508.
44. Linton PJ, Harbertson J, Bradley LM. A critical role for B cells in the development of memory CD4 cells. J Immunol 2000; 165: 5558-5565.
45. Lund FE, Hollifield M, Schuer K, Lines JL, Randall TD, Garvy BA. B cells are required for generation of protective effector and memory CD4 cells in response to Pneumocystis lung infection. J Immunol 2006; 176: 6147-6154.
46. Serreze DV, Fleming SA, Chapman HD, Richard SD, Leiter EH, Tisch RM. B lymphocytes are critical antigen-presenting cells for the initiation of T cell-mediated autoimmune diabetes in nonobese diabetic mice. J Immunol 1998; 161: 3912-3918.
47. Saadoun D, Rosenzwajg M, Landau D, Piette JC, Klatzmann D, Cacoub P. Restoration of peripheral immune homeostasis after rituximab in mixed cryoglobulinemia vasculitis. Blood 2008; 111: 5334-5341.
48. Sfikakis PP, Souliotis VL, Fragiadaki KG, Moutsopoulos HM, Boletis JN, Theofilopoulos AN. Increased expression of the FoxP3 functional marker of regulatory T cells following B cell depletion with rituximab in patients with lupus nephritis. Clin Immunol 2007; 123: 66-73.
49. Lund FE, Randall TD. Effector and regulatory B cells: modulators of CD4(+) T cell immunity. Nat Rev Immunol 2010; 10: 236-247.
50. Dhirapong A, Lleo A, Yang GX, Tsuneyama K, Dunn R, Kehry M, et al. B cell depletion therapy exacerbates murine primary biliary cirrhosis. HEPATOLOGY 2011; 53: 527-535.