Theoretical Analysis of the Evolution of Immune Memory

Overview

Journal BMC Evol Biol

Publisher Biomed Central

Specialty Biology

Date 2010 Dec 15

PMID 21143840

Citations 7

Authors

Frederik Graw

Carsten Magnus

Roland R Regoes

Affiliations

Soon will be listed here.

Abstract

Background: The ability of an immune system to remember pathogens improves the chance of the host to survive a second exposure to the same pathogen. This immunological memory has evolved in response to the pathogen environment of the hosts. In vertebrates, the memory of previous infection is physiologically accomplished by the development of memory T and B cells. Many questions concerning the generation and maintenance of immunological memory are still debated. Is there a limit to how many memory cells a host can generate and maintain? If there is a limit, how should new cells be incorporated into a filled memory compartment? And how many different pathogens should the immune system remember?

Results: In this study, we examine how memory traits evolve as a response to different pathogen environments using an individual-based model. We find that even without a cost related to the maintenance of a memory pool, the positive effect of bigger memory pool sizes saturates. The optimal diversity of a limited memory pool is determined by the probability of re-infection, rather than by the prevalence of a pathogen in the environment, or the frequency of exposure.

Conclusions: Relating immune memory traits to the pathogen environment of the hosts, our population biological framework sheds light on the evolutionary determinants of immune memory.

Citing Articles

Exploring immune memory traits in the social immunity of a fungus-growing ant.

Goes A, Kooij P, Haifig I, Bueno O, Rodrigues A Proc Biol Sci. 2024; 291(2037):20241097.

PMID: 39689882 PMC: 11651894. DOI: 10.1098/rspb.2024.1097.

Cell-Free Filtrates (CFF) as Vectors of a Transmissible Pathologic Tissue Memory Code: A Hypothetical and Narrative Review.

Berlanga-Acosta J, Fernandez-Mayola M, Mendoza-Mari Y, Garcia-Ojalvo A, Martinez-Jimenez I, Rodriguez-Rodriguez N Int J Mol Sci. 2022; 23(19).

PMID: 36232877 PMC: 9570059. DOI: 10.3390/ijms231911575.

Disentangling non-specific and specific transgenerational immune priming components in host-parasite interactions.

Ben-Ami F, Orlic C, Regoes R Proc Biol Sci. 2020; 287(1920):20192386.

PMID: 32075526 PMC: 7031663. DOI: 10.1098/rspb.2019.2386.

Cell-intrinsic regulation of peripheral memory-phenotype T cell frequencies.

Chawla A, Kanodia P, Mukherjee A, Jain V, Kaur G, Coshic P PLoS One. 2018; 13(12):e0200227.

PMID: 30557341 PMC: 6296671. DOI: 10.1371/journal.pone.0200227.

The evolution of costly acquired immune memory.

Best A, Hoyle A Ecol Evol. 2013; 3(7):2223-32.

PMID: 23919164 PMC: 3728959. DOI: 10.1002/ece3.611.

References

Selin L, Lin M, Kraemer K, Pardoll D, Schneck J, Varga S . Attrition of T cell memory: selective loss of LCMV epitope-specific memory CD8 T cells following infections with heterologous viruses. Immunity. 2000; 11(6):733-42. DOI: 10.1016/s1074-7613(00)80147-8. View

Huster K, Stemberger C, Gasteiger G, Kastenmuller W, Drexler I, Busch D . Cutting edge: memory CD8 T cell compartment grows in size with immunological experience but nevertheless can lose function. J Immunol. 2009; 183(11):6898-902. DOI: 10.4049/jimmunol.0902454. View

de Boer R, Oprea M, Antia R, Ahmed R, Perelson A . Recruitment times, proliferation, and apoptosis rates during the CD8(+) T-cell response to lymphocytic choriomeningitis virus. J Virol. 2001; 75(22):10663-9. PMC: 114648. DOI: 10.1128/JVI.75.22.10663-10669.2001. View

Marrack P, Bender J, Hildeman D, Jordan M, Mitchell T, Murakami M . Homeostasis of alpha beta TCR+ T cells. Nat Immunol. 2001; 1(2):107-11. DOI: 10.1038/77778. View

Schmidt N, Podyminogin R, Butler N, Badovinac V, Tucker B, Bahjat K . Memory CD8 T cell responses exceeding a large but definable threshold provide long-term immunity to malaria. Proc Natl Acad Sci U S A. 2008; 105(37):14017-22. PMC: 2544571. DOI: 10.1073/pnas.0805452105. View

Cooper M, Herrin B . How did our complex immune system evolve?. Nat Rev Immunol. 2009; 10(1):2-3. DOI: 10.1038/nri2686. View

Freitas A, Rocha B . Population biology of lymphocytes: the flight for survival. Annu Rev Immunol. 2000; 18:83-111. DOI: 10.1146/annurev.immunol.18.1.83. View

Antia R, Pilyugin S, Ahmed R . Models of immune memory: on the role of cross-reactive stimulation, competition, and homeostasis in maintaining immune memory. Proc Natl Acad Sci U S A. 1998; 95(25):14926-31. PMC: 24552. DOI: 10.1073/pnas.95.25.14926. View

Kaech S, Tan J, Wherry E, Konieczny B, Surh C, Ahmed R . Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat Immunol. 2003; 4(12):1191-8. DOI: 10.1038/ni1009. View

10.

Lau L, Sambhara S, Lemonnier F, Altman J, Ahmed R . Persistence of memory CD8 T cells in MHC class I-deficient mice. Science. 1999; 286(5443):1377-81. DOI: 10.1126/science.286.5443.1377. View

11.

Miller M, White A, Boots M . Host life span and the evolution of resistance characteristics. Evolution. 2007; 61(1):2-14. DOI: 10.1111/j.1558-5646.2007.00001.x. View

12.

Fazekas de St Groth , Webster R . Disquisitions of Original Antigenic Sin. I. Evidence in man. J Exp Med. 1966; 124(3):331-45. PMC: 2138235. DOI: 10.1084/jem.124.3.331. View

13.

Stemberger C, Huster K, Koffler M, Anderl F, Schiemann M, Wagner H . A single naive CD8+ T cell precursor can develop into diverse effector and memory subsets. Immunity. 2007; 27(6):985-97. DOI: 10.1016/j.immuni.2007.10.012. View

14.

Smith D, Dudani R, Pedras-Vasconcelos J, Chapdelaine Y, van Faassen H, Sad S . Cross-reactive antigen is required to prevent erosion of established T cell memory and tumor immunity: a heterologous bacterial model of attrition. J Immunol. 2002; 169(3):1197-206. DOI: 10.4049/jimmunol.169.3.1197. View

15.

Fellay J, Ge D, Shianna K, Colombo S, Ledergerber B, Cirulli E . Common genetic variation and the control of HIV-1 in humans. PLoS Genet. 2009; 5(12):e1000791. PMC: 2791220. DOI: 10.1371/journal.pgen.1000791. View

16.

Sadd B, Schmid-Hempel P . Insect immunity shows specificity in protection upon secondary pathogen exposure. Curr Biol. 2006; 16(12):1206-10. DOI: 10.1016/j.cub.2006.04.047. View

17.

Gaudin E, Rosado M, Agenes F, McLean A, Freitas A . B-cell homeostasis, competition, resources, and positive selection by self-antigens. Immunol Rev. 2004; 197:102-15. DOI: 10.1111/j.0105-2896.2004.0095.x. View

18.

Taylor L, Latham S, Woolhouse M . Risk factors for human disease emergence. Philos Trans R Soc Lond B Biol Sci. 2001; 356(1411):983-9. PMC: 1088493. DOI: 10.1098/rstb.2001.0888. View

19.

McLean A . Modelling T cell memory. J Theor Biol. 1994; 170(1):63-74. DOI: 10.1006/jtbi.1994.1168. View

20.

Harty J, Badovinac V . Shaping and reshaping CD8+ T-cell memory. Nat Rev Immunol. 2008; 8(2):107-19. DOI: 10.1038/nri2251. View