Programmed Cell Death-1 Pathway Deficiency Enhances Autoimmunity Leading to Dacryoadenitis of Mice
Programmed cell death protein (PD)-1 is a coinhibitory molecule that suppresses immune response and maintains immune homeostasis. Moreover, the PD-1 pathway blocks cancers from being attacked by immune cells. Anti–PD-1 antibody therapy such as nivolumab improves survival in cancer patients. However,...
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| Published in | The American journal of pathology Vol. 191; no. 6; pp. 1077 - 1093 |
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| Main Authors | , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
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United States
Elsevier Inc
01.06.2021
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| Abstract | Programmed cell death protein (PD)-1 is a coinhibitory molecule that suppresses immune response and maintains immune homeostasis. Moreover, the PD-1 pathway blocks cancers from being attacked by immune cells. Anti–PD-1 antibody therapy such as nivolumab improves survival in cancer patients. However, the occurrence of autoimmune inflammatory disorders in various organs has been increasingly reported as an adverse effect of nivolumab. Of the disorders associated with nivolumab, Sicca syndrome occurs in 3% to 11% of cases and has unknown pathologic mechanisms. Whether the absence of the PD-1 pathway causes functional and morphologic disorders in lacrimal glands was determined by analyzing PD-1 gene–knockout (Pdcd1−/−) mice. Histopathologic analysis showed that Pdcd1−/− mice developed dacryoadenitis beginning at 3 to 4 months of age, and deteriorated with age. Flow-cytometric analysis confirmed that cells infiltrating the affected lacrimal glands consisted mainly of CD3+ T cells and only a small proportion of CD19+ B cells. Among infiltrating T cells, the CD4+ Th-cell subset consisted of Th1 cells producing interferon-γ in an early stage of dacryoadenitis in Pdcd1−/− mice. Experiments of lymphocyte transfer from Pdcd1−/− into irradiated wild-type mice confirmed that CD4+ T cells from Pdcd1−/− mice induced dacryoadenitis. These results indicate that PD-1 plays an important role in the prevention of autoimmune inflammatory disorders in lacrimal glands caused by activated CD4+ Th1 cells. |
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| AbstractList | Programmed cell death protein (PD)-1 is a coinhibitory molecule that suppresses immune response and maintains immune homeostasis. Moreover, the PD-1 pathway blocks cancers from being attacked by immune cells. Anti-PD-1 antibody therapy such as nivolumab improves survival in cancer patients. However, the occurrence of autoimmune inflammatory disorders in various organs has been increasingly reported as an adverse effect of nivolumab. Among them, sicca syndrome occurs in 3% to 11% with unknown pathologic mechanisms. Whether the absence of the PD-1 pathway causes functional and morphologic disorders in lacrimal glands was determined by analyzing PD-1 gene-knockout (Pdcd1
) mice. Histopathologic analysis showed that Pdcd1
mice developed dacryoadenitis beginning at 3 to 4 months of age, and deteriorated with age. Flow-cytometric analysis confirmed that cells infiltrating the affected lacrimal glands consisted mainly of CD3
T cells and only a small proportion of CD19
B cells. Among infiltrating T cells, the CD4
Th-cell subset consisted of Th1 cells producing interferon-γ in an early stage of dacryoadenitis in Pdcd1
mice. Experiments of lymphocyte transfer from Pdcd1
into irradiated wild-type mice confirmed that CD4
T cells from Pdcd1
mice induced dacryoadenitis. These results indicate that PD-1 plays an important role in the prevention of autoimmune inflammatory disorders in lacrimal glands caused by activated CD4
Th1 cells. Programmed cell death protein (PD)-1 is a coinhibitory molecule that suppresses immune response and maintains immune homeostasis. Moreover, the PD-1 pathway blocks cancers from being attacked by immune cells. Anti–PD-1 antibody therapy such as nivolumab improves survival in cancer patients. However, the occurrence of autoimmune inflammatory disorders in various organs has been increasingly reported as an adverse effect of nivolumab. Of the disorders associated with nivolumab, Sicca syndrome occurs in 3% to 11% of cases and has unknown pathologic mechanisms. Whether the absence of the PD-1 pathway causes functional and morphologic disorders in lacrimal glands was determined by analyzing PD-1 gene–knockout (Pdcd1−/−) mice. Histopathologic analysis showed that Pdcd1−/− mice developed dacryoadenitis beginning at 3 to 4 months of age, and deteriorated with age. Flow-cytometric analysis confirmed that cells infiltrating the affected lacrimal glands consisted mainly of CD3+ T cells and only a small proportion of CD19+ B cells. Among infiltrating T cells, the CD4+ Th-cell subset consisted of Th1 cells producing interferon-γ in an early stage of dacryoadenitis in Pdcd1−/− mice. Experiments of lymphocyte transfer from Pdcd1−/− into irradiated wild-type mice confirmed that CD4+ T cells from Pdcd1−/− mice induced dacryoadenitis. These results indicate that PD-1 plays an important role in the prevention of autoimmune inflammatory disorders in lacrimal glands caused by activated CD4+ Th1 cells. |
| Author | Saitoh, Daizoh Karasawa, Yoko Takeuchi, Masaru Takayama, Kei Goto, Hiroshi Sakurai, Yutaka Hattori, Takaaki Usui, Yoshihiko Ito, Masataka Nishio, Yoshiaki Yamakawa, Naoyuki |
| Author_xml | – sequence: 1 givenname: Yutaka orcidid: 0000-0002-2426-5439 surname: Sakurai fullname: Sakurai, Yutaka email: ysaku@ndmc.ac.jp organization: Department of Ophthalmology, National Defense Medical College, Saitama, Japan – sequence: 2 givenname: Yoshihiko surname: Usui fullname: Usui, Yoshihiko organization: Department of Ophthalmology, Tokyo Medical University, Tokyo, Japan – sequence: 3 givenname: Takaaki surname: Hattori fullname: Hattori, Takaaki organization: Department of Ophthalmology, Tokyo Medical University, Tokyo, Japan – sequence: 4 givenname: Masaru surname: Takeuchi fullname: Takeuchi, Masaru organization: Department of Ophthalmology, National Defense Medical College, Saitama, Japan – sequence: 5 givenname: Kei surname: Takayama fullname: Takayama, Kei organization: Department of Ophthalmology, National Defense Medical College, Saitama, Japan – sequence: 6 givenname: Yoko surname: Karasawa fullname: Karasawa, Yoko organization: Department of Ophthalmology, National Defense Medical College, Saitama, Japan – sequence: 7 givenname: Yoshiaki surname: Nishio fullname: Nishio, Yoshiaki organization: Department of Ophthalmology, National Defense Medical College, Saitama, Japan – sequence: 8 givenname: Naoyuki surname: Yamakawa fullname: Yamakawa, Naoyuki organization: Department of Ophthalmology, Tokyo Medical University, Tokyo, Japan – sequence: 9 givenname: Daizoh surname: Saitoh fullname: Saitoh, Daizoh organization: Division of Traumatology, Research Institute, National Defense Medical College, Saitama, Japan – sequence: 10 givenname: Hiroshi surname: Goto fullname: Goto, Hiroshi organization: Department of Ophthalmology, Tokyo Medical University, Tokyo, Japan – sequence: 11 givenname: Masataka surname: Ito fullname: Ito, Masataka email: masataka@ndmc.ac.jp organization: Department of Developmental Anatomy and Regenerative Biology, National Defense Medical College, Saitama, Japan |
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