Journal Article
. 2017 May; 8:513.
doi: 10.3389/fimmu.2017.00513.

Comparative Analysis of Immune Checkpoint Molecules and Their Potential Role in the Transmissible Tasmanian Devil Facial Tumor Disease

Andrew S Flies 1 Nicholas B Blackburn 1 Alan Bruce Lyons 2 John D Hayball 3 Gregory M Woods 1 
  • PMID: 28515726
  •     211 References
  •     7 citations


Immune checkpoint molecules function as a system of checks and balances that enhance or inhibit immune responses to infectious agents, foreign tissues, and cancerous cells. Immunotherapies that target immune checkpoint molecules, particularly the inhibitory molecules programmed cell death 1 and cytotoxic T-lymphocyte-associated protein 4 (CTLA-4), have revolutionized human oncology in recent years, yet little is known about these key immune signaling molecules in species other than primates and rodents. The Tasmanian devil facial tumor disease is caused by transmissible cancers that have resulted in a massive decline in the wild Tasmanian devil population. We have recently demonstrated that the inhibitory checkpoint molecule PD-L1 is upregulated on Tasmanian devil (Sarcophilus harrisii) facial tumor cells in response to the interferon-gamma cytokine. As this could play a role in immune evasion by tumor cells, we performed a thorough comparative analysis of checkpoint molecule protein sequences among Tasmanian devils and eight other species. We report that many of the key signaling motifs and ligand-binding sites in the checkpoint molecules are highly conserved across the estimated 162 million years of evolution since the last common ancestor of placental and non-placental mammals. Specifically, we discovered that the CTLA-4 (MYPPPY) ligand-binding motif and the CTLA-4 (GVYVKM) inhibitory domain are completely conserved across all nine species used in our comparative analysis, suggesting that the function of CTLA-4 is likely conserved in these species. We also found that cysteine residues for intra- and intermolecular disulfide bonds were also highly conserved. For instance, all 20 cysteine residues involved in disulfide bonds in the human 4-1BB molecule were also present in devil 4-1BB. Although many key sequences were conserved, we have also identified immunoreceptor tyrosine-based inhibitory motifs (ITIMs) and immunoreceptor tyrosine-based switch motifs (ITSMs) in genes and protein domains that have not been previously reported in any species. This checkpoint molecule analysis and review of salient features for each of the molecules presented here can serve as road map for the development of a Tasmanian devil facial tumor disease immunotherapy. Finally, the strategies can be used as a guide for veterinarians, ecologists, and other researchers willing to venture into the nascent field of wild immunology.

Keywords: allograft; checkpoint blockade; cosignaling immunotherapy; devil; evolution; transmissible tumor; transplant rejection; wild immunity.

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PLoS One, 2012 Nov 13; 7(11). PMID: 23144904    Free PMC article.
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Immunity, 2003 Jun 24; 18(6). PMID: 12818165
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Nature, 2001 Mar 30; 410(6828). PMID: 11279502
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A comparative overview of immunoglobulin genes and the generation of their diversity in tetrapods.
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Hui Wang, Jon VerHalen, +6 authors, Yong-Guang Yang.
Blood, 2006 Sep 30; 109(2). PMID: 17008545    Free PMC article.
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Immunity, 2003 Jun 24; 18(6). PMID: 12818166
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J C Schwartz, X Zhang, +2 authors, S C Almo.
Nature, 2001 Mar 30; 410(6828). PMID: 11279501
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J Immunol, 1999 Oct 08; 163(8). PMID: 10510357
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Immunity, 2007 Mar 17; 26(3). PMID: 17363302
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J Immunol, 2001 Apr 21; 166(9). PMID: 11313386
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CD47 fusion protein targets CD172a+ cells in Crohn's disease and dampens the production of IL-1β and TNF.
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J Exp Med, 2013 May 15; 210(6). PMID: 23669395    Free PMC article.
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J Exp Med, 2010 Sep 08; 207(10). PMID: 20819923    Free PMC article.
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Y J Kim, K E Pollok, +4 authors, B S Kwon.
J Immunol, 1993 Aug 01; 151(3). PMID: 8335927
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Ana C Anderson, Sheng Xiao, Vijay K Kuchroo.
Immunity, 2007 Mar 23; 26(3). PMID: 17376389
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Blood, 2003 May 31; 102(6). PMID: 12775570
Human Soluble CD80 is generated by alternative splicing, and recombinant soluble CD80 binds to CD28 and CD152 influencing T-cell activation.
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Scand J Immunol, 2007 Oct 24; 66(5). PMID: 17953528
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Cell, 2015 Apr 11; 161(2). PMID: 25860608    Free PMC article.
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Cancer stem cells, CD200 and immunoevasion.
Brian T Kawasaki, William L Farrar.
Trends Immunol, 2008 Sep 09; 29(10). PMID: 18775673
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Immunity, 2016 May 19; 44(5). PMID: 27192563    Free PMC article.
Highly Cited. Review.
Molecular cloning and sequencing of canine T-cell costimulatory molecule (CD28).
T S Khatlani, Z Ma, M Okuda, T Onishi.
Vet Immunol Immunopathol, 2001 Apr 09; 78(3-4). PMID: 11292534
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Sci Transl Med, 2010 Dec 24; 2(63). PMID: 21178137    Free PMC article.
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Vet Res, 2013 Jul 24; 44. PMID: 23876077    Free PMC article.
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Mol Immunol, 2008 Dec 17; 46(3). PMID: 19081138
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S J Coles, R K Hills, +4 authors, A Tonks.
Leukemia, 2012 Mar 21; 26(9). PMID: 22430636    Free PMC article.
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Infect Immun, 2016 Jul 20; 84(10). PMID: 27430272    Free PMC article.
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Phase III randomized clinical trial comparing tremelimumab with standard-of-care chemotherapy in patients with advanced melanoma.
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J Clin Oncol, 2013 Jan 09; 31(5). PMID: 23295794    Free PMC article.
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Highly Cited. Review.
SHP-1 and SHP-2 associate with immunoreceptor tyrosine-based switch motif of programmed death 1 upon primary human T cell stimulation, but only receptor ligation prevents T cell activation.
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J Immunol, 2004 Jul 09; 173(2). PMID: 15240681
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Increased expression of the LGALS3 (galectin 3) gene in human non-small-cell lung cancer.
Akinobu Yoshimura, Akihiko Gemma, +12 authors, Shoji Kudoh.
Genes Chromosomes Cancer, 2003 Apr 16; 37(2). PMID: 12696064
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Dev Comp Immunol, 2006 Aug 25; 31(3). PMID: 16928399
Integrin-associated protein: a 50-kD plasma membrane antigen physically and functionally associated with integrins.
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Phylogenetic divergence of CD47 interactions with human signal regulatory protein alpha reveals locus of species specificity. Implications for the binding site.
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J Biol Chem, 2006 Nov 14; 282(3). PMID: 17098740
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CD137 ligand mediates opposite effects in human and mouse NK cells and impairs NK-cell reactivity against human acute myeloid leukemia cells.
Tina Baessler, Jean Enno Charton, +5 authors, Helmut Rainer Salih.
Blood, 2009 Dec 17; 115(15). PMID: 20008791
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Proc Natl Acad Sci U S A, 2007 Mar 16; 104(12). PMID: 17360380    Free PMC article.
Feline programmed death and its ligand: characterization and changes with feline immunodeficiency virus infection.
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Coexpression of Tim-3 and PD-1 identifies a CD8+ T-cell exhaustion phenotype in mice with disseminated acute myelogenous leukemia.
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Blood, 2011 Mar 10; 117(17). PMID: 21385853    Free PMC article.
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Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti-CTLA-4 therapy against melanoma.
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A novel system to map protein interactions reveals evolutionarily conserved immune evasion pathways on transmissible cancers.
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