Adaptation to low parasite abundance affects immune investment and immunopathological responses of cavefish.
Journal
Nature ecology & evolution
ISSN: 2397-334X
Titre abrégé: Nat Ecol Evol
Pays: England
ID NLM: 101698577
Informations de publication
Date de publication:
10 2020
10 2020
Historique:
received:
19
12
2019
accepted:
22
05
2020
pubmed:
22
7
2020
medline:
15
12
2020
entrez:
22
7
2020
Statut:
ppublish
Résumé
Reduced parasitic infection rates in the developed world are suspected to underlie the rising prevalence of autoimmune disorders. However, the long-term evolutionary consequences of decreased parasite exposure on an immune system are not well understood. We used the Mexican tetra Astyanax mexicanus to understand how loss of parasite diversity influences the evolutionary trajectory of the vertebrate immune system, by comparing river with cave morphotypes. Here, we present field data affirming a strong reduction in parasite diversity in the cave ecosystem, and show that cavefish immune cells display a more sensitive pro-inflammatory response towards bacterial endotoxins. Surprisingly, other innate cellular immune responses, such as phagocytosis, are drastically decreased in cavefish. Using two independent single-cell approaches, we identified a shift in the overall immune cell composition in cavefish as the underlying cellular mechanism, indicating strong differences in the immune investment strategy. While surface fish invest evenly into the innate and adaptive immune systems, cavefish shifted immune investment to the adaptive immune system, and here, mainly towards specific T-cell populations that promote homeostasis. Additionally, inflammatory responses and immunopathological phenotypes in visceral adipose tissue are drastically reduced in cavefish. Our data indicate that long-term adaptation to low parasite diversity coincides with a more sensitive immune system in cavefish, which is accompanied by a reduction in the immune cells that play a role in mediating the pro-inflammatory response.
Identifiants
pubmed: 32690906
doi: 10.1038/s41559-020-1234-2
pii: 10.1038/s41559-020-1234-2
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
1416-1430Subventions
Organisme : NIGMS NIH HHS
ID : R01 GM127872
Pays : United States
Références
The Global Burden of Disease: 2004 Update (WHO, 2004).
Sheldon, B. C. & Verhulst, S. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol. Evol. 11, 317–321 (1996).
pubmed: 21237861
Schmid-Hempel, P. Variation in immune defence as a question of evolutionary ecology. Proc. R. Soc. B. 270, 357–366 (2003).
pubmed: 12639314
Schmid-Hempel, P. Evolutionary Parasitology (Oxford Univ. Press, 2013).
Rook, G. A. Regulation of the immune system by biodiversity from the natural environment: an ecosystem service essential to health. Proc. Natl Acad. Sci. USA 110, 18360–18367 (2013).
pubmed: 24154724
von Hertzen, L., Hanski, I. & Haahtela, T. Natural immunity. Biodiversity loss and inflammatory diseases are two global megatrends that might be related. EMBO Rep. 12, 1089–1093 (2011).
Belkaid, Y. & Hand, T. W. Role of the microbiota in immunity and inflammation. Cell 157, 121–141 (2014).
pubmed: 24679531
pmcid: 4056765
Lambrecht, B. N. & Hammad, H. The immunology of the allergy epidemic and the hygiene hypothesis. Nat. Immunol. 18, 1076–1083 (2017).
pubmed: 28926539
Rook, G. A., Martinelli, R. & Brunet, L. R. Innate immune responses to mycobacteria and the downregulation of atopic responses. Curr. Opin. Allergy Clin. Immunol. 3, 337–342 (2003).
pubmed: 14501431
Rosenblum, M. D., Remedios, K. A. & Abbas, A. K. Mechanisms of human autoimmunity. J. Clin. Invest. 125, 2228–2233 (2015).
pubmed: 25893595
pmcid: 4518692
Lafferty, K. D. Biodiversity loss decreases parasite diversity: theory and patterns. Philos. Trans. R. Soc. Lond. B 367, 2814–2827 (2012).
Kamiya, T., O’Dwyer, K., Nakagawa, S. & Poulin, R. Host diversity drives parasite diversity: meta-analytical insights into patterns and causal mechanisms. Ecography 37, 689–697 (2014).
McDade, T. W., Georgiev, A. V. & Kuzawa, C. W. Trade-offs between acquired and innate immune defenses in humans. Evol. Med. Public Health 2016, 1–16 (2016).
pubmed: 26739325
pmcid: 4703052
Lindstrom, K. M., Foufopoulos, J., Parn, H. & Wikelski, M. Immunological investments reflect parasite abundance in island populations of Darwin’s finches. Proc. R. Soc. B 271, 1513–1519 (2004).
pubmed: 15306324
Mayer, A., Mora, T., Rivoire, O. & Walczak, A. M. Diversity of immune strategies explained by adaptation to pathogen statistics. Proc. Natl Acad. Sci. USA 113, 8630–8635 (2016).
pubmed: 27432970
Scharsack, J. P., Kalbe, M., Harrod, C. & Rauch, G. Habitat-specific adaptation of immune responses of stickleback (Gasterosteus aculeatus) lake and river ecotypes. Proc. R. Soc. B 274, 1523–1532 (2007).
pubmed: 17426014
Kaczorowski, K. J. et al. Continuous immunotypes describe human immune variation and predict diverse responses. Proc. Natl Acad. Sci. USA 114, E6097–E6106 (2017).
pubmed: 28696306
Herman, A. et al. The role of gene flow in rapid and repeated evolution of cave-related traits in Mexican tetra, Astyanax mexicanus. Mol. Ecol. 27, 4397–4416 (2018).
pubmed: 30252986
pmcid: 6261294
Fumey, J. et al. Evidence for late Pleistocene origin of Astyanax mexicanus cavefish. BMC Evol. Biol. 18, 43 (2018).
pubmed: 29665771
pmcid: 5905186
Gibert, J. & Deharveng, L. Subterranean ecosystems: a truncated functional biodiversity. BioScience 52, 473–481 (2002).
Tabin, J. A. et al. Temperature preference of cave and surface populations of Astyanax mexicanus. Dev. Biol. 441, 338–344 (2018).
pubmed: 29704470
pmcid: 6119108
Abolins, S. et al. The comparative immunology of wild and laboratory mice, Mus musculus domesticus. Nat. Commun. 8, 14811 (2017).
pubmed: 28466840
pmcid: 5418598
Trama, A. M. et al. Lymphocyte phenotypes in wild-caught rats suggest potential mechanisms underlying increased immune sensitivity in post-industrial environments. Cell Mol. Immunol. 9, 163–174 (2012).
pubmed: 22327212
pmcid: 3719982
Aspiras, A. C., Rohner, N., Martineau, B., Borowsky, R. L. & Tabin, C. J. Melanocortin 4 receptor mutations contribute to the adaptation of cavefish to nutrient-poor conditions. Proc. Natl Acad. Sci. USA 112, 9668–9673 (2015).
pubmed: 26170297
Xiong, S., Krishnan, J., Peuss, R. & Rohner, N. Early adipogenesis contributes to excess fat accumulation in cave populations of Astyanax mexicanus. Dev. Biol. 441, 297–304 (2018).
pubmed: 29883659
Wiens, G. D. & Vallejo, R. L. Temporal and pathogen-load dependent changes in rainbow trout (Oncorhynchus mykiss) immune response traits following challenge with biotype 2 Yersinia ruckeri. Fish Shellfish Immunol. 29, 639–647 (2010).
pubmed: 20600959
Krishnan, J. et al. Comparative transcriptome analysis of wild and lab populations of Astyanax mexicanus uncovers differential effects of environment and morphotype on gene expression. J. Exp. Zool. B https://doi.org/10.1002/jez.b.22933 (2020).
Moller, A. M., Korytar, T., Kollner, B., Schmidt-Posthaus, H. & Segner, H. The teleostean liver as an immunological organ: intrahepatic immune cells (IHICs) in healthy and benzo[a]pyrene challenged rainbow trout (Oncorhynchus mykiss). Dev. Comp. Immunol. 46, 518–529 (2014).
pubmed: 24718255
Traver, D. et al. Transplantation and in vivo imaging of multilineage engraftment in zebrafish bloodless mutants. Nat. Immunol. 4, 1238–1246 (2003).
pubmed: 14608381
Stockdale, W. T. et al. Heart regeneration in the Mexican cavefish. Cell Rep. 25, 1997–2007 (2018).
pubmed: 30462998
pmcid: 6280125
Ramsey, S. et al. Transcriptional noise and cellular heterogeneity in mammalian macrophages. Philos. Trans. R. Soc. Lond. B. 361, 495–506 (2006).
Ogryzko, N. V., Renshaw, S. A. & Wilson, H. L. The IL-1 family in fish: swimming through the muddy waters of inflammasome evolution. Dev. Comp. Immunol. 46, 53–62 (2014).
Wittamer, V., Bertrand, J. Y., Gutschow, P. W. & Traver, D. Characterization of the mononuclear phagocyte system in zebrafish. Blood 117, 7126–7135 (2011).
pubmed: 21406720
Sunyer, J. O. Evolutionary and functional relationships of B cells from fish and mammals: Insights into their novel roles in phagocytosis and presentation of particulate antigen. Infect. Disord. Drug Targets 12, 200–212 (2012).
pubmed: 22394174
pmcid: 3420344
Lugo-Villarino, G. et al. Identification of dendritic antigen-presenting cells in the zebrafish. Proc. Natl Acad. Sci. USA 107, 15850–15855 (2010).
pubmed: 20733076
Haugland, G. T. et al. Phagocytosis and respiratory burst activity in lumpsucker (Cyclopterus lumpus L.) leucocytes analysed by flow cytometry. PLoS ONE 7, e47909 (2012).
pubmed: 23112870
pmcid: 3480447
Lieschke, G. J. & Trede, N. S. Fish immunology. Curr. Biol. 19, R678–R682 (2009).
pubmed: 19706273
Balla, K. M. et al. Eosinophils in the zebrafish: prospective isolation, characterization, and eosinophilia induction by helminth determinants. Blood 116, 3944–3954 (2010).
pubmed: 20713961
pmcid: 2981543
Bolnick, D. I., Shim, K. C., Schmerer, M. & Brock, C. D. Population-specific covariation between immune function and color of nesting male threespine stickleback. PLoS ONE 10, e0126000 (2015).
pubmed: 26039044
pmcid: 4454680
Peuß, R. et al. Label-independent flow cytometry and unsupervised neural network method for de novo clustering of cell populations. Preprint at bioRxiv https://doi.org/10.1101/603035 (2020).
van der Meer, W., Scott, C. S. & de Keijzer, M. H. Automated flagging influences the inconsistency and bias of band cell and atypical lymphocyte morphological differentials. Clin. Chem. Lab. Med. 42, 371–377 (2004).
pubmed: 15147145
Getz, G. S. Thematic review series: the immune system and atherogenesis. Bridging the innate and adaptive immune systems. J. Lipid Res. 46, 619–622 (2005).
pubmed: 15722562
Wan, F. et al. Characterization of gammadelta T cells from zebrafish provides insights into their important role in adaptive humoral immunity. Front. Immunol. 7, 675 (2016).
pubmed: 28119690
Shilpi, Paul,S. & Lal, G. Role of gamma-delta (gammadelta) T cells in autoimmunity. J. Leukoc. Biol. 97, 259–271 (2015).
pubmed: 25502468
Fan, X. & Rudensky, A. Y. Hallmarks of tissue-resident lymphocytes. Cell 164, 1198–1211 (2016).
pubmed: 26967286
pmcid: 4973889
Papotto, P. H., Reinhardt, A., Prinz, I. & Silva-Santos, B. Innately versatile: gammadelta17 T cells in inflammatory and autoimmune diseases. J. Autoimmun. 87, 26–37 (2018).
pubmed: 29203226
Fay, N. S., Larson, E. C. & Jameson, J. M. Chronic Inflammation and gammadelta T. Cells Front. Immunol. 7, 210 (2016).
pubmed: 27303404
Rossi, D. J. et al. Cell intrinsic alterations underlie hematopoietic stem cell aging. Proc. Natl Acad. Sci. USA 102, 9194–9199 (2005).
pubmed: 15967997
Bolli, N. et al. Expression of the cytoplasmic NPM1 mutant (NPMc
pubmed: 20197555
pmcid: 2858496
Stachura, D. L. et al. Clonal analysis of hematopoietic progenitor cells in the zebrafish. Blood 118, 1274–1282 (2011).
pubmed: 21415264
pmcid: 3152495
Reavie, L. et al. Regulation of hematopoietic stem cell differentiation by a single ubiquitin ligase-substrate complex. Nat. Immunol. 11, 207–215 (2010).
pubmed: 20081848
pmcid: 2825759
Cabezas-Wallscheid, N. et al. Identification of regulatory networks in HSCs and their immediate progeny via integrated proteome, transcriptome, and DNA methylome analysis. Cell Stem Cell 15, 507–522 (2014).
Cheng, J. et al. Hematopoietic defects in mice lacking the sialomucin CD34. Blood 87, 479–490 (1996).
pubmed: 8555469
Anjos-Afonso, F. et al. CD34(
Amin, R. H. & Schlissel, M. S. Foxo1 directly regulates the transcription of recombination-activating genes during B cell development. Nat. Immunol. 9, 613–622 (2008).
pubmed: 18469817
pmcid: 2612116
Han, S., Zheng, B., Schatz, D. G., Spanopoulou, E. & Kelsoe, G. Neoteny in lymphocytes: Rag1 and Rag2 expression in germinal center B cells. Science 274, 2094–2097 (1996).
pubmed: 8953043
Naito, Y. et al. Germinal center marker GL7 probes activation-dependent repression of N-glycolylneuraminic acid, a sialic acid species involved in the negative modulation of B-cell activation. Mol. Cell Biol. 27, 3008–3022 (2007).
pubmed: 17296732
pmcid: 1899932
Laszlo, G., Hathcock, K. S., Dickler, H. B. & Hodes, R. J. Characterization of a novel cell-surface molecule expressed on subpopulations of activated T and B cells. J. Immunol. 150, 5252–5262 (1993).
pubmed: 8515058
Fänge, R. & Nilsson, S. The fish spleen: structure and function. Experientia 41, 152–158 (1985).
pubmed: 3972063
Steinel, N. C. & Bolnick, D. I. Melanomacrophage centers as a histological indicator of immune function in fish and other poikilotherms. Front. Immunol. 8, 827 (2017).
pubmed: 28769932
pmcid: 5512340
Cervenak, L., Magyar, A., Boja, R. & Laszlo, G. Differential expression of GL7 activation antigen on bone marrow B cell subpopulations and peripheral B cells. Immunol. Lett. 78, 89–96 (2001).
pubmed: 11672592
Secombes, C. J., Wang, T. & Bird, S. The interleukins of fish. Dev. Comp. Immunol. 35, 1336–1345 (2011).
pubmed: 21605591
Weisberg, S. P. et al. Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 112, 1796–1808 (2003).
pubmed: 14679176
pmcid: 296995
Christ, A. et al. Western diet triggers NLRP3-dependent innate immune reprogramming. Cell 172, 162–175 e114 (2018).
pubmed: 29328911
pmcid: 6324559
McAlpine, C. S. et al. Sleep modulates haematopoiesis and protects against atherosclerosis. Nature 566, 383–387 (2019).
Heidt, T. et al. Chronic variable stress activates hematopoietic stem cells. Nat. Med. 20, 754–758 (2014).
pubmed: 24952646
pmcid: 4087061
Mitchell, R. G., Russell, W. H. & Elliott, W. R. Mexican Eyeless Characin Fishes, Genus Astyanax: Environment, Distribution, and Evolution (Texas Tech Press, 1977).
Espinasa, L. et al. A new cave locality for Astyanax cavefish in Sierra de El Abra, Mexico. Subterr. Biol. 26, 39–53 (2018).
Embryo Surface Sanitation (Egg Bleaching) Protocol https://zebrafish.org/wiki/protocols/ess (ZIRC, 2019).
Peuß, R., Eggert, H., Armitage, S. A. & Kurtz, J. Downregulation of the evolutionary capacitor Hsp90 is mediated by social cues. Proc. R. Soc. B 282, 20152041 (2015).
pubmed: 26582024
Pfaffl, M. W., Horgan, G. W. & Dempfle, L. Relative expression software tool (REST(C)) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30, 36e (2002).
Zhang, Y. A. et al. IgT, a primitive immunoglobulin class specialized in mucosal immunity. Nat. Immunol. 11, 827–835 (2010).
pubmed: 20676094
pmcid: 3459821
Rowe, R. G., Mandelbaum, J., Zon, L. I. & Daley, G. Q. Engineering hematopoietic stem cells: lessons from development. Cell Stem Cell 18, 707–720 (2016).
pubmed: 27257760
pmcid: 4911194
Stachura, D. L. et al. The zebrafish granulocyte colony-stimulating factors (Gcsfs): 2 paralogous cytokines and their roles in hematopoietic development and maintenance. Blood 122, 3918–3928 (2013).
pubmed: 24128862
pmcid: 3854111
de Jong, J. L. & Zon, L. I. Use of the zebrafish system to study primitive and definitive hematopoiesis. Ann. Rev. Genet. 39, 481–501 (2005).
pubmed: 16285869
Athanasiadis, E. I. et al. Single-cell RNA-sequencing uncovers transcriptional states and fate decisions in haematopoiesis. Nat. Commun. 8, 2045 (2017).
pubmed: 29229905
pmcid: 5725498
Zeng, A. et al. Prospectively isolated tetraspanin(
pubmed: 29906446
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
Sun, K. et al. Endotrophin triggers adipose tissue fibrosis and metabolic dysfunction. Nat. Commun. 5, 3485 (2014).
pubmed: 24647224
pmcid: 4076823
R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2014).
Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57, 289–300 (1995).