Dual nature of the adaptive immune system in lampreys
Open accessAbstract
Jawless vertebrates use variable lymphocyte receptors (VLR) comprised of leucine-rich-repeat (LRR) segments as counterparts of the immunoglobulin-based receptors that jawed vertebrates use for antigen recognition. Highly diverse VLR genes are somatically assembled by the insertion of variable LRR sequences into incomplete germline VLRA and VLRB genes. Here we show that in sea lampreys (Petromyzon marinus) VLRA and VLRB anticipatory receptors are expressed by separate lymphocyte populations by monoallelic VLRA or VLRB assembly, together with expression of cytosine deaminase 1 (CDA1) or 2 (CDA2), respectively. Distinctive gene expression profiles for VLRA(+) and VLRB(+) lymphocytes resemble those of mammalian T and B cells. Although both the VLRA and the VLRB cells proliferate in response to antigenic stimulation, only the VLRB lymphocytes bind native antigens and differentiate into VLR antibody-secreting cells. Conversely, VLRA lymphocytes respond preferentially to a classical T-cell mitogen and upregulate the expression of the pro-inflammatory cytokine genes interleukin-17 (IL-17) and macrophage migration inhibitory factor (MIF). The finding of T-like and B-like lymphocytes in lampreys offers new insight into the evolution of adaptive immunity.
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In immune cells, a variety of effector genes is controlled by the same familiar sets of regulatory genes across diverse strategies.
“Immune cells provide the most evidence, for as knowledge of the diverse strategies for immune response, both adaptive and non-adaptive, extends beyond mammals, an amazing variety of effector genes is revealed but the same familiar sets of regulatory genes are found to control their expression.”
From Evolution of Gene Regulatory Networks Controlling Body Plan Development (2011) · cites this paper as Guo et al., 2009
The ‘Distinctive gene expression profiles’ section reports that lamprey lymphocytes express transcription factors also associated with T cells in jawed vertebrates, alongside cytokines and other immune genes (page not provided). This supports a narrower claim about shared regulatory genes across two adaptive immune systems. It does not establish that those genes control the effector genes’ expression or extend the finding to non-adaptive immune strategies. (LLM, conf=0.84)
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References 50 · Cited by 336
- Authors
- Guo, P., Hirano, M., Herrin, B. R., Li, J., Yu, C., Sadlonova, A., & Cooper, M. D.
- Affiliations
- Emory University (US)
- Corresponding author
- Cooper, Max D.
- Venue
- Nature
- Published
- 2009-05-27
- Volume
- 459
- Issue
- 7248
- Pages
- 796-801
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC2714547
- OpenAlex
- W2167855218
- Cited by
- 336
- References
- 50
- Citations by year
- 2026: 13 · 2025: 6 · 2024: 14 · 2023: 6 · 2022: 8 · 2021: 18 · 2020: 19 · 2019: 12 · 2018: 18 · 2017: 19 · 2016: 22 · 2015: 21 · 2014: 24 · 2013: 33 · 2012: 26
- FWCI
- 14.78
- Type
- journal article
- Language
- en
- Update notices
- erratum (2009-08-20)
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Institute of Allergy and Infectious Diseases (T32AI007051, R01AI072435)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Life Sciences › Immunology and Microbiology › Immunology › Aquaculture disease management and microbiota
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Keywords
- sea lamprey, variable lymphocyte receptors, leucine-rich repeat receptors, jawless fishes, cytosine deaminase, IL-17, macrophage migration inhibitory factor, antigen recognition, lymphocyte differentiation, antibody-secreting cells
- MeSH terms
- Alleles, Animals, Antigens, Biological Evolution, Lampreys, Lymphocytes, Macrophage Migration-Inhibitory Factors, Mitogens, Phytohemagglutinins, Receptors, Immunologic, Interleukin-17, Amino Acid Motifs, Gene Expression Profiling, Fish Proteins, Cytosine Deaminase
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