{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,27]],"date-time":"2026-02-27T03:55:59Z","timestamp":1772164559654,"version":"3.50.1"},"reference-count":45,"publisher":"American Association for Cancer Research (AACR)","issue":"9","content-domain":{"domain":["aacrjournals.org"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[2013,5,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Purpose: Identify subgroups of patients with relapsed\/refractory follicular lymphoma deriving substantial progression-free survival (PFS) benefit with bortezomib\u2013rituximab versus rituximab in the phase III LYM-3001 study.<\/jats:p>\n                  <jats:p>Experimental Design: A total of 676 patients were randomized to five 5-week cycles of bortezomib\u2013rituximab or rituximab. The primary end point was PFS; this prespecified analysis of candidate protein biomarkers and genes was an exploratory objective. Archived tumor tissue and whole blood samples were collected at baseline. Immunohistochemistry and genetic analyses were completed for 4 proteins and 8 genes.<\/jats:p>\n                  <jats:p>Results: In initial pairwise analyses, using individual single-nucleotide polymorphism genotypes, one biomarker pair (PSMB1 P11A C\/G heterozygote, low CD68 expression) was associated with a significant PFS benefit with bortezomib\u2013rituximab versus rituximab, controlling for multiple comparison corrections. The pair was analyzed under dominant, recessive, and additive genetic models, with significant association with PFS seen under the dominant model (G\/G+C\/G). In patients carrying this biomarker pair [PSMB1 P11A G allele, low CD68 expression (\u226450 CD68-positive cells), population frequency: 43.6%], median PFS was 14.2 months with bortezomib\u2013rituximab versus 9.1 months with rituximab (HR 0.47, P &amp;lt; 0.0001), and there was a significant overall survival benefit (HR 0.49, P = 0.0461). Response rates were higher and time to next antilymphoma therapy was longer in the bortezomib\u2013rituximab group. In biomarker-negative patients, no significant efficacy differences were seen between treatment groups. Similar proportions of patients had high-risk features in the biomarker-positive and biomarker-negative subsets.<\/jats:p>\n                  <jats:p>Conclusions: Patients with PSMB1 P11A (G allele) and low CD68 expression seemed to have significantly longer PFS and greater clinical benefit with bortezomib\u2013rituximab versus rituximab. Clin Cancer Res; 19(9); 2551\u201361. \u00a92013 AACR.<\/jats:p>","DOI":"10.1158\/1078-0432.ccr-12-3069","type":"journal-article","created":{"date-parts":[[2013,4,2]],"date-time":"2013-04-02T23:54:13Z","timestamp":1364946853000},"page":"2551-2561","update-policy":"https:\/\/doi.org\/10.1158\/crossmark_policy","source":"Crossref","is-referenced-by-count":13,"title":["Prespecified Candidate Biomarkers Identify Follicular Lymphoma Patients Who Achieved Longer Progression-Free Survival with Bortezomib\u2013Rituximab Versus Rituximab"],"prefix":"10.1158","volume":"19","author":[{"given":"Bertrand","family":"Coiffier","sequence":"first","affiliation":[{"name":"Authors' Affiliations:\u20081H\u00e9matologie, Hospices Civils de Lyon and University Lyon 1, Lyon, France; 2Janssen Research and Development, Spring House, Pennsylvania; 3Janssen Research and Development, Raritan, New Jersey; 4David Geffen School of Medicine at the University of California and Translational Oncology Research International, Los Angeles, California; 5Millennium Pharmaceuticals, Inc., Cambridge, Massachusetts; 6Janssen Research and Development, High Wycombe; 7Department of Haematology, Derriford Hospital, Plymouth, United Kingdom; 8Dienst Hematologie, UZ Gent, Gent, Belgium; 9Janssen Research and Development, Beerse, Belgium; 10Cancer Research Center, Moscow, Russia; 11Cancer Hospital, FuDan University, Shanghai, China; 12Instituto Nacional de C\u00e2ncer, Rio de Janeiro, Brazil; 13CEITEC Brno, and Department of Internal Medicine, Hematology and Oncology, University Hospital Brno and School of Medicine, Masaryk University, Brno, Czech Republic; 14Hospitais da Universidade de Coimbra, Coimbra, Portugal; 15The"}]},{"given":"Weimin","family":"Li","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081H\u00e9matologie, Hospices Civils de Lyon and University Lyon 1, Lyon, France; 2Janssen Research and Development, Spring House, Pennsylvania; 3Janssen Research and Development, Raritan, New Jersey; 4David Geffen School of Medicine at the University of California and Translational Oncology Research International, Los Angeles, California; 5Millennium Pharmaceuticals, Inc., Cambridge, Massachusetts; 6Janssen Research and Development, High Wycombe; 7Department of Haematology, Derriford Hospital, Plymouth, United Kingdom; 8Dienst Hematologie, UZ Gent, Gent, Belgium; 9Janssen Research and Development, Beerse, Belgium; 10Cancer Research Center, Moscow, Russia; 11Cancer Hospital, FuDan University, Shanghai, China; 12Instituto Nacional de C\u00e2ncer, Rio de Janeiro, Brazil; 13CEITEC Brno, and Department of Internal Medicine, Hematology and Oncology, University Hospital Brno and School of Medicine, Masaryk University, Brno, Czech Republic; 14Hospitais da Universidade de Coimbra, Coimbra, Portugal; 15The"}]},{"given":"Erin D.","family":"Henitz","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081H\u00e9matologie, Hospices Civils de Lyon and University Lyon 1, Lyon, France; 2Janssen Research and Development, Spring House, Pennsylvania; 3Janssen Research and Development, Raritan, New Jersey; 4David Geffen School of Medicine at the University of California and Translational Oncology Research International, Los Angeles, California; 5Millennium Pharmaceuticals, Inc., Cambridge, Massachusetts; 6Janssen Research and Development, High Wycombe; 7Department of Haematology, Derriford Hospital, Plymouth, United Kingdom; 8Dienst Hematologie, UZ Gent, Gent, Belgium; 9Janssen Research and Development, Beerse, Belgium; 10Cancer Research Center, Moscow, Russia; 11Cancer Hospital, FuDan University, Shanghai, China; 12Instituto Nacional de C\u00e2ncer, Rio de Janeiro, Brazil; 13CEITEC Brno, and Department of Internal Medicine, Hematology and Oncology, University Hospital Brno and School of Medicine, Masaryk University, Brno, Czech Republic; 14Hospitais da Universidade de Coimbra, Coimbra, Portugal; 15The"}]},{"given":"Jayaprakash D.","family":"Karkera","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081H\u00e9matologie, Hospices Civils de Lyon and University Lyon 1, Lyon, France; 2Janssen Research and Development, Spring House, Pennsylvania; 3Janssen Research and Development, Raritan, New Jersey; 4David Geffen School of Medicine at the University of California and Translational Oncology Research International, Los Angeles, California; 5Millennium Pharmaceuticals, Inc., Cambridge, Massachusetts; 6Janssen Research and Development, High Wycombe; 7Department of Haematology, Derriford Hospital, Plymouth, United Kingdom; 8Dienst Hematologie, UZ Gent, Gent, Belgium; 9Janssen Research and Development, Beerse, Belgium; 10Cancer Research Center, Moscow, Russia; 11Cancer Hospital, FuDan University, Shanghai, China; 12Instituto Nacional de C\u00e2ncer, Rio de Janeiro, Brazil; 13CEITEC Brno, and Department of Internal Medicine, Hematology and Oncology, University Hospital Brno and School of Medicine, Masaryk University, Brno, Czech Republic; 14Hospitais da Universidade de Coimbra, Coimbra, Portugal; 15The"}]},{"given":"Reyna","family":"Favis","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081H\u00e9matologie, Hospices Civils de Lyon and University Lyon 1, Lyon, France; 2Janssen Research and Development, Spring House, Pennsylvania; 3Janssen Research and Development, Raritan, New Jersey; 4David Geffen School of Medicine at the University of California and Translational Oncology Research International, Los Angeles, California; 5Millennium Pharmaceuticals, Inc., Cambridge, Massachusetts; 6Janssen Research and Development, High Wycombe; 7Department of Haematology, Derriford Hospital, Plymouth, United Kingdom; 8Dienst Hematologie, UZ Gent, Gent, Belgium; 9Janssen Research and Development, Beerse, Belgium; 10Cancer Research Center, Moscow, Russia; 11Cancer Hospital, FuDan University, Shanghai, China; 12Instituto Nacional de C\u00e2ncer, Rio de Janeiro, Brazil; 13CEITEC Brno, and Department of Internal Medicine, Hematology and Oncology, University Hospital Brno and School of Medicine, Masaryk University, Brno, Czech Republic; 14Hospitais da Universidade de Coimbra, Coimbra, Portugal; 15The"}]},{"given":"Dana","family":"Gaffney","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081H\u00e9matologie, Hospices Civils de Lyon and University Lyon 1, Lyon, France; 2Janssen Research and Development, Spring House, Pennsylvania; 3Janssen Research and Development, Raritan, New Jersey; 4David Geffen School of Medicine at the University of California and Translational Oncology Research International, Los Angeles, California; 5Millennium Pharmaceuticals, Inc., Cambridge, Massachusetts; 6Janssen Research and Development, High Wycombe; 7Department of Haematology, Derriford Hospital, Plymouth, United Kingdom; 8Dienst Hematologie, UZ Gent, Gent, Belgium; 9Janssen Research and Development, Beerse, Belgium; 10Cancer Research Center, Moscow, Russia; 11Cancer Hospital, FuDan University, Shanghai, China; 12Instituto Nacional de C\u00e2ncer, Rio de Janeiro, Brazil; 13CEITEC Brno, and Department of Internal Medicine, Hematology and Oncology, University Hospital Brno and School of Medicine, Masaryk University, Brno, Czech Republic; 14Hospitais da Universidade de Coimbra, Coimbra, Portugal; 15The"}]},{"given":"Alice","family":"Shapiro","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081H\u00e9matologie, Hospices Civils de Lyon and University Lyon 1, Lyon, France; 2Janssen Research and Development, Spring House, Pennsylvania; 3Janssen Research and Development, Raritan, New Jersey; 4David Geffen School of Medicine at the University of California and Translational Oncology Research International, Los Angeles, California; 5Millennium Pharmaceuticals, Inc., Cambridge, Massachusetts; 6Janssen Research and Development, High Wycombe; 7Department of Haematology, Derriford Hospital, Plymouth, United Kingdom; 8Dienst Hematologie, UZ Gent, Gent, Belgium; 9Janssen Research and Development, Beerse, Belgium; 10Cancer Research Center, Moscow, Russia; 11Cancer Hospital, FuDan University, Shanghai, China; 12Instituto Nacional de C\u00e2ncer, Rio de Janeiro, Brazil; 13CEITEC Brno, and Department of Internal Medicine, Hematology and Oncology, University Hospital Brno and School of Medicine, Masaryk University, Brno, Czech Republic; 14Hospitais da Universidade de Coimbra, Coimbra, Portugal; 15The"}]},{"given":"Panteli","family":"Theocharous","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081H\u00e9matologie, Hospices Civils de Lyon and University Lyon 1, Lyon, France; 2Janssen Research and Development, Spring House, Pennsylvania; 3Janssen Research and Development, Raritan, New Jersey; 4David Geffen School of Medicine at the University of California and Translational Oncology Research International, Los Angeles, California; 5Millennium Pharmaceuticals, Inc., Cambridge, Massachusetts; 6Janssen Research and Development, High Wycombe; 7Department of Haematology, Derriford Hospital, Plymouth, United Kingdom; 8Dienst Hematologie, UZ Gent, Gent, Belgium; 9Janssen Research and Development, Beerse, Belgium; 10Cancer Research Center, Moscow, Russia; 11Cancer Hospital, FuDan University, Shanghai, China; 12Instituto Nacional de C\u00e2ncer, Rio de Janeiro, Brazil; 13CEITEC Brno, and Department of Internal Medicine, Hematology and Oncology, University Hospital Brno and School of Medicine, Masaryk University, Brno, Czech Republic; 14Hospitais da Universidade de Coimbra, Coimbra, Portugal; 15The"}]},{"given":"Yusri A.","family":"Elsayed","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081H\u00e9matologie, Hospices Civils de Lyon and University Lyon 1, Lyon, France; 2Janssen Research and Development, Spring House, Pennsylvania; 3Janssen Research and Development, Raritan, New Jersey; 4David Geffen School of Medicine at the University of California and Translational Oncology Research International, Los Angeles, California; 5Millennium Pharmaceuticals, Inc., Cambridge, Massachusetts; 6Janssen Research and Development, High Wycombe; 7Department of Haematology, Derriford Hospital, Plymouth, United Kingdom; 8Dienst Hematologie, UZ Gent, Gent, Belgium; 9Janssen Research and Development, Beerse, Belgium; 10Cancer Research Center, Moscow, Russia; 11Cancer Hospital, FuDan University, Shanghai, China; 12Instituto Nacional de C\u00e2ncer, Rio de Janeiro, Brazil; 13CEITEC Brno, and Department of Internal Medicine, Hematology and Oncology, University Hospital Brno and School of Medicine, Masaryk University, Brno, Czech Republic; 14Hospitais da Universidade de Coimbra, Coimbra, Portugal; 15The"}]},{"given":"Helgi","family":"van de Velde","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081H\u00e9matologie, Hospices Civils de Lyon and University Lyon 1, Lyon, France; 2Janssen Research and Development, Spring House, Pennsylvania; 3Janssen Research and Development, Raritan, New Jersey; 4David Geffen School of Medicine at the University of California and Translational Oncology Research International, Los Angeles, California; 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5Millennium Pharmaceuticals, Inc., Cambridge, Massachusetts; 6Janssen Research and Development, High Wycombe; 7Department of Haematology, Derriford Hospital, Plymouth, United Kingdom; 8Dienst Hematologie, UZ Gent, Gent, Belgium; 9Janssen Research and Development, Beerse, Belgium; 10Cancer Research Center, Moscow, Russia; 11Cancer Hospital, FuDan University, Shanghai, China; 12Instituto Nacional de C\u00e2ncer, Rio de Janeiro, Brazil; 13CEITEC Brno, and Department of Internal Medicine, Hematology and Oncology, University Hospital Brno and School of Medicine, Masaryk University, Brno, Czech Republic; 14Hospitais da Universidade de Coimbra, Coimbra, Portugal; 15The"}]},{"given":"Adriana","family":"Scheliga","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081H\u00e9matologie, Hospices Civils de Lyon and University Lyon 1, Lyon, France; 2Janssen Research and Development, Spring House, Pennsylvania; 3Janssen Research and Development, Raritan, New Jersey; 4David Geffen School of Medicine at the University of California and Translational Oncology Research International, Los Angeles, California; 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5Millennium Pharmaceuticals, Inc., Cambridge, Massachusetts; 6Janssen Research and Development, High Wycombe; 7Department of Haematology, Derriford Hospital, Plymouth, United Kingdom; 8Dienst Hematologie, UZ Gent, Gent, Belgium; 9Janssen Research and Development, Beerse, Belgium; 10Cancer Research Center, Moscow, Russia; 11Cancer Hospital, FuDan University, Shanghai, China; 12Instituto Nacional de C\u00e2ncer, Rio de Janeiro, Brazil; 13CEITEC Brno, and Department of Internal Medicine, Hematology and Oncology, University Hospital Brno and School of Medicine, Masaryk University, Brno, Czech Republic; 14Hospitais da Universidade de Coimbra, Coimbra, Portugal; 15The"}]},{"given":"Adriana","family":"Teixeira","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081H\u00e9matologie, Hospices Civils de Lyon and University Lyon 1, Lyon, France; 2Janssen Research and Development, Spring House, Pennsylvania; 3Janssen Research and Development, Raritan, New Jersey; 4David Geffen School of Medicine at the University of California and Translational Oncology Research International, Los Angeles, California; 5Millennium Pharmaceuticals, Inc., Cambridge, Massachusetts; 6Janssen Research and Development, High Wycombe; 7Department of Haematology, Derriford Hospital, Plymouth, United Kingdom; 8Dienst Hematologie, UZ Gent, Gent, Belgium; 9Janssen Research and Development, Beerse, Belgium; 10Cancer Research Center, Moscow, Russia; 11Cancer Hospital, FuDan University, Shanghai, China; 12Instituto Nacional de C\u00e2ncer, Rio de Janeiro, Brazil; 13CEITEC Brno, and Department of Internal Medicine, Hematology and Oncology, University Hospital Brno and School of Medicine, Masaryk University, Brno, Czech Republic; 14Hospitais da Universidade de Coimbra, Coimbra, Portugal; 15The"}]},{"given":"Joanna","family":"Romejko-Jarosinska","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081H\u00e9matologie, Hospices Civils de Lyon and University Lyon 1, Lyon, France; 2Janssen Research and Development, Spring House, Pennsylvania; 3Janssen Research and Development, Raritan, New Jersey; 4David Geffen School of Medicine at the University of California and Translational Oncology Research International, Los Angeles, California; 5Millennium Pharmaceuticals, Inc., Cambridge, Massachusetts; 6Janssen Research and Development, High Wycombe; 7Department of Haematology, Derriford Hospital, Plymouth, United Kingdom; 8Dienst Hematologie, UZ Gent, Gent, Belgium; 9Janssen Research and Development, Beerse, Belgium; 10Cancer Research Center, Moscow, Russia; 11Cancer Hospital, FuDan University, Shanghai, China; 12Instituto Nacional de C\u00e2ncer, Rio de Janeiro, Brazil; 13CEITEC Brno, and Department of Internal Medicine, Hematology and Oncology, University Hospital Brno and School of Medicine, Masaryk University, Brno, Czech Republic; 14Hospitais da Universidade de Coimbra, Coimbra, Portugal; 15The"}]},{"given":"Sven","family":"de Vos","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081H\u00e9matologie, Hospices Civils de Lyon and University Lyon 1, Lyon, France; 2Janssen Research and Development, Spring House, Pennsylvania; 3Janssen Research and Development, Raritan, New Jersey; 4David Geffen School of Medicine at the University of California and Translational Oncology Research International, Los Angeles, California; 5Millennium Pharmaceuticals, Inc., Cambridge, Massachusetts; 6Janssen Research and Development, High Wycombe; 7Department of Haematology, Derriford Hospital, Plymouth, United Kingdom; 8Dienst Hematologie, UZ Gent, Gent, Belgium; 9Janssen Research and Development, Beerse, Belgium; 10Cancer Research Center, Moscow, Russia; 11Cancer Hospital, FuDan University, Shanghai, China; 12Instituto Nacional de C\u00e2ncer, Rio de Janeiro, Brazil; 13CEITEC Brno, and Department of Internal Medicine, Hematology and Oncology, University Hospital Brno and School of Medicine, Masaryk University, Brno, Czech Republic; 14Hospitais da Universidade de Coimbra, Coimbra, Portugal; 15The"}]},{"given":"Michael","family":"Crump","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081H\u00e9matologie, Hospices Civils de Lyon and University Lyon 1, Lyon, France; 2Janssen Research and Development, Spring House, Pennsylvania; 3Janssen Research and Development, Raritan, New Jersey; 4David Geffen School of Medicine at the University of California and Translational Oncology Research International, Los Angeles, California; 5Millennium Pharmaceuticals, Inc., Cambridge, Massachusetts; 6Janssen Research and Development, High Wycombe; 7Department of Haematology, Derriford Hospital, Plymouth, United Kingdom; 8Dienst Hematologie, UZ Gent, Gent, Belgium; 9Janssen Research and Development, Beerse, Belgium; 10Cancer Research Center, Moscow, Russia; 11Cancer Hospital, FuDan University, Shanghai, China; 12Instituto Nacional de C\u00e2ncer, Rio de Janeiro, Brazil; 13CEITEC Brno, and Department of Internal Medicine, Hematology and Oncology, University Hospital Brno and School of Medicine, Masaryk University, Brno, Czech Republic; 14Hospitais da Universidade de Coimbra, Coimbra, Portugal; 15The"}]},{"given":"Ofer","family":"Shpilberg","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081H\u00e9matologie, Hospices Civils de Lyon and University Lyon 1, Lyon, France; 2Janssen Research and Development, Spring House, Pennsylvania; 3Janssen Research and Development, Raritan, New Jersey; 4David Geffen School of Medicine at the University of California and Translational Oncology Research International, Los Angeles, California; 5Millennium Pharmaceuticals, Inc., Cambridge, Massachusetts; 6Janssen Research and Development, High Wycombe; 7Department of Haematology, Derriford Hospital, Plymouth, United Kingdom; 8Dienst Hematologie, UZ Gent, Gent, Belgium; 9Janssen Research and Development, Beerse, Belgium; 10Cancer Research Center, Moscow, Russia; 11Cancer Hospital, FuDan University, Shanghai, China; 12Instituto Nacional de C\u00e2ncer, Rio de Janeiro, Brazil; 13CEITEC Brno, and Department of Internal Medicine, Hematology and Oncology, University Hospital Brno and School of Medicine, Masaryk University, Brno, Czech Republic; 14Hospitais da Universidade de Coimbra, Coimbra, Portugal; 15The"}]},{"given":"Pier Luigi","family":"Zinzani","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081H\u00e9matologie, Hospices Civils de Lyon and University Lyon 1, Lyon, France; 2Janssen Research and Development, Spring House, Pennsylvania; 3Janssen Research and Development, Raritan, New Jersey; 4David Geffen School of Medicine at the University of California and Translational Oncology Research International, Los Angeles, California; 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