The role of phagocytic cells in aging: insights from vertebrate and invertebrate models.
Aging
Coelomocyte
Granulocyte
Macrophage
Phagocytosis
Plasmatocyte
Journal
Biogerontology
ISSN: 1573-6768
Titre abrégé: Biogerontology
Pays: Netherlands
ID NLM: 100930043
Informations de publication
Date de publication:
21 Aug 2024
21 Aug 2024
Historique:
received:
03
07
2024
accepted:
12
08
2024
medline:
22
8
2024
pubmed:
22
8
2024
entrez:
21
8
2024
Statut:
aheadofprint
Résumé
While the main role of phagocytic scavenger cells consists of the neutralization and elimination of pathogens, they also keep the body fluids clean by taking up and breaking down waste material. Since a build-up of waste is thought to contribute to the aging process, these cells become particularly pertinent in the research field of aging. Nevertheless, a direct link between their scavenging functions and the aging process has yet to be established. Integrative approaches involving various model organisms hold promise to elucidate this potential, but are lagging behind since the diversity and evolutionary relationship of these cells across animal species remain unclear. In this perspective, we review the current knowledge associating phagocytic scavenger cells with aging in vertebrate and invertebrate animals, as well as put forward important questions for further exploration. Additionally, we highlight future challenges and propose a constructive approach for tackling them.
Identifiants
pubmed: 39168928
doi: 10.1007/s10522-024-10131-9
pii: 10.1007/s10522-024-10131-9
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Fonds Wetenschappelijk Onderzoek
ID : G049321N
Organisme : KU Leuven
ID : C16/19/003
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer Nature B.V.
Références
Adamo SA, Jensen M, Younger M (2001) Changes in lifetime immunocompetence in male and female Gryllus texensis (formerly G. integer): trade-offs between immunity and reproduction. Anim Behav 62:417–425. https://doi.org/10.1006/anbe.2001.1786
Akai H, Sato S (1973) Ultrastructure of the larval hemocytes of the silkworm, Bombyx mori L. (Lepidoptera: Bombycidae). Int J Insect Morphol Embryol 2:207–231. https://doi.org/10.1016/0020-7322(73)90029-9
Almanzar N, Antony J, Baghel AS et al (2020) A single-cell transcriptomic atlas characterizes ageing tissues in the mouse. Nature 583:590–595. https://doi.org/10.1038/s41586-020-2496-1
Altun ZF, Hall DH (2009) Coelomocyte system. WormAtlas. https://doi.org/10.3908/wormatlas.1.11
Amdam GV, Page RE (2005) Intergenerational transfers may have decoupled physiological and chronological age in a eusocial insect. Ageing Res Rev 4:398. https://doi.org/10.1016/J.ARR.2005.03.007
pubmed: 16039913
pmcid: 2398690
Amdam GV, Simões ZLP, Hagen A et al (2004) Hormonal control of the yolk precursor vitellogenin regulates immune function and longevity in honeybees. Exp Gerontol 39:767–773. https://doi.org/10.1016/J.EXGER.2004.02.010
pubmed: 15130671
Amdam GV, Aase ALTO, Seehuus SC et al (2005) Social reversal of immunosenescence in honey bee workers. Exp Gerontol 40:939. https://doi.org/10.1016/J.EXGER.2005.08.004
pubmed: 16169181
pmcid: 2409152
Anisimova AA, Diagileva MN, Sinenko AV, Dmitrieva IA (2023) Age-related and seasonal dynamics of the hemocyte population in the Mussel Crenomytilus grayanus (Dunker, 1853). Russ J Mar Biol 49:106–118. https://doi.org/10.1134/S1063074023020025
Aprahamian T, Takemura Y, Goukassian D, Walsh K (2008) Ageing is associated with diminished apoptotic cell clearance in vivo. Clin Exp Immunol 152:448–455. https://doi.org/10.1111/j.1365-2249.2008.03658.x
pubmed: 18422728
pmcid: 2453212
Arnardottir HH, Dalli J, Colas RA et al (2014) Aging delays resolution of acute in ammation in mice: reprogramming the host response with novel nano-proresolving medicines. J Immunol 193:8. https://doi.org/10.4049/jimmunol.1401313
Arroyo Portilla C, Tomas J, Gorvel JP, Lelouard H (2021) From species to regional and local specialization of intestinal macrophages. Front Cell Dev Biol 8:624213. https://doi.org/10.3389/fcell.2020.624213
pubmed: 33681185
pmcid: 7930007
Bednaski AV, Trevisan-Silva D, Matsubara FH et al (2015) Characterization of Brown spider (Loxosceles intermedia) hemolymph: cellular and biochemical analyses. Toxicon 98:62–74. https://doi.org/10.1016/j.toxicon.2015.02.008
pubmed: 25720299
Bergmans S, Raes L, Moons L, De GL (2023) A review on neurodegeneration in the fast-ageing killifish, the first animal model to study the natural occurrence of neuronal cell loss. Ageing Res Rev 91:102065. https://doi.org/10.1016/j.arr.2023.102065
pubmed: 37666433
Bodnar AG, Coffman JA (2016) Maintenance of somatic tissue regeneration with age in short- and long-lived species of sea urchins. Aging Cell 15:778–787. https://doi.org/10.1111/acel.12487
pubmed: 27095483
pmcid: 4933669
Bolla RI, Weinstein PP, Cain GD (1972) Fine structure of the coelomocyte of adult Ascaris suum. J Parasitol 58:1025. https://doi.org/10.2307/3278127
pubmed: 4345109
Bouallegui Y (2021) A comprehensive review on crustaceans’ immune system with a focus on freshwater crayfish in relation to crayfish plague disease. Front Immunol 12:667787. https://doi.org/10.3389/fimmu.2021.667787
pubmed: 34054837
pmcid: 8155518
Britton C, Laing R, McNeilly TN et al (2023) New technologies to study helminth development and host-parasite interactions. Int J Parasitol 53:393–403. https://doi.org/10.1016/j.ijpara.2022.11.012
pubmed: 36931423
Buchmann K (2014) Evolution of innate immunity: clues from invertebrates via fish to mammals. Front Immunol 5:459. https://doi.org/10.3389/fimmu.2014.00459
pubmed: 25295041
pmcid: 4172062
Buis A, Bellemin S, Goudeau J et al (2019) Coelomocytes regulate starvation-induced fat catabolism and lifespan extension through the lipase LIPL-5 in Caenorhabditis elegans. Cell Rep 28:1041-1049.e4. https://doi.org/10.1016/j.celrep.2019.06.064
pubmed: 31340142
pmcid: 6667774
Bump P, Lubeck L (2023) Marine invertebrates one cell at a time: insights from single-cell analysis. Integr Comp Biol 63:999–1009. https://doi.org/10.1093/icb/icad034
pubmed: 37188638
pmcid: 10714908
Butcher S, Chahel H, Mrc JML et al (2000) Ageing and the neutrophil: no appetite for killing? Immunology 100:411–416. https://doi.org/10.1046/j.1365-2567.2000.00079.x
pubmed: 10929066
pmcid: 2327031
Camacho-Pereira J, Tarragó MG, Chini CCS et al (2016) CD38 dictates age-related NAD decline and mitochondrial dysfunction through an SIRT3-dependent mechanism. Cell Metab 23:1127–1139. https://doi.org/10.1016/j.cmet.2016.05.006
pubmed: 27304511
pmcid: 4911708
Carballal MJ, Villalba A, López C (1998) Seasonal variation and effects of age, food availability, size, gonadal development, and parasitism on the hemogram of Mytilus galloprovincialis. J Invertebr Pathol 72:304–312. https://doi.org/10.1006/jipa.1998.4779
pubmed: 9784355
Carneiro MC, Henriques CM, Nabais J et al (2016) Short telomeres in key tissues initiate local and systemic aging in Zebrafish. PLoS Genet 12:1–31. https://doi.org/10.1371/journal.pgen.1005798
Castelein N, Cai H, Rasulova M, Braeckman BP (2014) Lifespan regulation under axenic dietary restriction: a close look at the usual suspects. Exp Gerontol 58:96–103. https://doi.org/10.1016/j.exger.2014.07.015
pubmed: 25066271
Castillo JC, Robertson AE, Strand MR (2006) Characterization of hemocytes from the mosquitoes Anopheles gambiae and Aedes aegypti. Insect Biochem Mol Biol 36:891–903. https://doi.org/10.1016/j.ibmb.2006.08.010
pubmed: 17098164
pmcid: 2757042
Chia F-S, Xing J (1996) Echinoderm coelomocytes. Zool Stud 35:231–254
Christensen BM, Huff BM, Miranpuri GS et al (1989) Hemocyte population changes during the immune response of Aedes aegypti to inoculated microfilariae of Dirofilaria immitis. J Parasitol 75:119–123. https://doi.org/10.2307/3282948
pubmed: 2918431
Cypser JR, Kitzenberg D, Park S (2013) Dietary restriction in C. elegans: recent advances. Exp Gerontol 48:1014–1017. https://doi.org/10.1016/j.exger.2013.02.018
pubmed: 23462461
David DC, Ollikainen N, Trinidad JC et al (2010) Widespread protein aggregation as an inherent part of aging in C. elegans. PLoS Biol 8:e1000450. https://doi.org/10.1371/journal.pbio.1000450
pubmed: 20711477
pmcid: 2919420
Davis BM, Salinas-Navarro M, Cordeiro MF et al (2017) Characterizing microglia activation: a spatial statistics approach to maximize information extraction. Sci Rep 7:1576. https://doi.org/10.1038/s41598-017-01747-8
pubmed: 28484229
pmcid: 5431479
De Maeyer RPH, Chambers ES (2021) The impact of ageing on monocytes and macrophages. Immunol Lett 230:1–10. https://doi.org/10.1016/j.imlet.2020.12.003
pubmed: 33309673
De Maeyer RPH, van de Merwe RC, Louie R et al (2020) Blocking elevated p38 MAPK restores efferocytosis and inflammatory resolution in the elderly. Nat Immunol 21:615–625. https://doi.org/10.1038/s41590-020-0646-0
pubmed: 32251403
pmcid: 7983074
de la Ballina NR, Maresca F, Cao A, Villalba A (2022) Bivalve haemocyte subpopulations: a review. Front Immunol 13:826255. https://doi.org/10.3389/fimmu.2022.826255
pubmed: 35464425
pmcid: 9024128
Doums C, Moret Y, Benelli E, Schmid-Hempel P (2002) Senescence of immune defence in Bombus workers. Ecol Entomol 27:138–144. https://doi.org/10.1046/J.1365-2311.2002.00388.X
Du C, Anderson A, Lortie M et al (2013) Oxidative damage and cellular defense mechanisms in sea urchin models of aging. Free Radic Biol Med 63:254–263. https://doi.org/10.1016/j.freeradbiomed.2013.05.023
pubmed: 23707327
pmcid: 3782381
Dubey M, Nagarkoti S, Awasthi D et al (2016) Nitric oxide-mediated apoptosis of neutrophils through caspase-8 and caspase-3-dependent mechanism. Cell Death Dis 7:1–12. https://doi.org/10.1038/cddis.2016.248
El Maï M, Bird M, Allouche A et al (2023) Gut-specific telomerase expression counteracts systemic aging in telomerase-deficient zebrafish. Nat Aging 3:567–584. https://doi.org/10.1038/s43587-023-00401-5
pubmed: 37142828
pmcid: 10191862
El Maï M, Marzullo M, de Castro IP et al (2020) Opposing p53 and mTOR/AKT promote an in vivo switch from apoptosis to senescence upon telomere shortening in zebrafish. Elife 9:1–26. https://doi.org/10.7554/elife.54935
Ezcurra M, Benedetto A, Sornda T et al (2018) C. elegans eats its own intestine to make yolk leading to multiple senescent pathologies. Curr Biol 28:2544-2556.e5. https://doi.org/10.1016/j.cub.2018.06.035
pubmed: 30100339
pmcid: 6108400
Fang EF, Lautrup S, Hou Y et al (2017) NAD+ in aging: molecular mechanisms and translational implications. Trends Mol Med 23:899–916. https://doi.org/10.1016/j.molmed.2017.08.001
pubmed: 28899755
pmcid: 7494058
Fares H, Greenwald I (2001) Genetic analysis of endocytosis in Caenorhabditis elegans: coelomocyte uptake defective mutants. Genetics 159:133–145. https://doi.org/10.1093/genetics/159.1.133
pubmed: 11560892
pmcid: 1461804
Franceschi C, Garagnani P, Vitale G et al (2017) Inflammaging and ‘Garb-aging.’ Trends Endocrinol Metab 28:199–212. https://doi.org/10.1016/j.tem.2016.09.005
pubmed: 27789101
Frisch BJ, Hoffman CM, Latchney SE et al (2019) Aged marrow macrophages expand platelet-biased hematopoietic stem cells via Interleukin1B. JCI Insight 5:e124213. https://doi.org/10.1172/jci.insight.124213
pubmed: 30998506
Gallotta I, Sandhu A, Peters M et al (2020) Extracellular proteostasis prevents aggregation during pathogenic attack. Nature 584:410–414. https://doi.org/10.1038/s41586-020-2461-z
pubmed: 32641833
Galván-Peña S, O’Neill LAJ (2014) Metabolic reprogramming in macrophage polarization. Front Immunol 5:1–6. https://doi.org/10.3389/fimmu.2014.00420
Garigan D, Hsu AL, Fraser AG et al (2002) Genetic analysis of tissue aging in Caenorhabditis elegans: a role for heat-shock factor and bacterial proliferation. Genetics 161:1101–1112. https://doi.org/10.1093/genetics/161.3.1101
pubmed: 12136014
pmcid: 1462187
Gems D, de la Guardia Y (2013) Alternative perspectives on aging in Caenorhabditis elegans: reactive oxygen species or hyperfunction? Antioxid Redox Signal 19:321–329. https://doi.org/10.1089/ars.2012.4840
pubmed: 22870907
pmcid: 5395017
Ghosh S, Ghosh S, Mandal L (2020) Drosophila metamorphosis involves hemocyte mediated macroendocytosis and efferocytosis. Int J Dev Biol 64:319–329. https://doi.org/10.1387/ijdb.190215lm
pubmed: 32658992
pmcid: 7612856
Gomes AP, Price NL, Ling AJY et al (2013) Declining NAD+ induces a pseudohypoxic state disrupting nuclear-mitochondrial communication during aging. Cell 155:1624–1638. https://doi.org/10.1016/j.cell.2013.11.037
pubmed: 24360282
pmcid: 4076149
Günther J, Seyfert HM (2018) The first line of defence: insights into mechanisms and relevance of phagocytosis in epithelial cells. Semin Immunopathol 40:555–565. https://doi.org/10.1007/s00281-018-0701-1
pubmed: 30182191
pmcid: 6223882
Herndon LA, Schmeissner PJ, Dudaronek JM et al (2002) Stochastic and genetic factors influence tissue-specific decline in ageing C. elegans. Nature 419:808–814. https://doi.org/10.1038/nature01135
pubmed: 12397350
Hillyer JF, Schmidt SL, Fuchs JF et al (2005) Age-associated mortality in immune challenged mosquitoes (Aedes aegypti) correlates with a decrease in haemocyte numbers. Cell Microbiol 7:39–51. https://doi.org/10.1111/J.1462-5822.2004.00430.X
pubmed: 15617522
Hirano M (2016) Echinoderm immunity: is the larval immune system immature? Immunol Cell Biol 94:809–811. https://doi.org/10.1038/icb.2016.67
pubmed: 27527904
Ho ECH, Buckley KM, Schrankel CS et al (2016) Perturbation of gut bacteria induces a coordinated cellular immune response in the purple sea urchin larva. Immunol Cell Biol 94:861–874. https://doi.org/10.1038/icb.2016.51
Hoeffel G, Chen J, Lavin Y et al (2015) C-Myb(+) erythro-myeloid progenitor-derived fetal monocytes give rise to adult tissue-resident macrophages. Immunity 42:665–678. https://doi.org/10.1016/j.immuni.2015.03.011
pubmed: 25902481
pmcid: 4545768
Horn L, Leips J, Starz-Gaiano M (2014) Phagocytic ability declines with age in adult Drosophila hemocytes. Aging Cell 13:719–728. https://doi.org/10.1111/ACEL.12227
pubmed: 24828474
pmcid: 4116448
Huang C, Wagner-Valladolid S, Stephens AD et al (2019) Intrinsically aggregation-prone proteins form amyloid-like aggregates and contribute to tissue aging in Caenorhabditis elegans. Elife 8:e43059. https://doi.org/10.7554/eLife.43059
pubmed: 31050339
pmcid: 6524967
Hultmark D, Andó I (2022) Hematopoietic plasticity mapped in Drosophila and other insects. Elife 11:e78906. https://doi.org/10.7554/eLife.78906
pubmed: 35920811
pmcid: 9348853
Hystad EM, Salmela H, Amdam GV, Münch D (2017) Hemocyte-mediated phagocytosis differs between honey bee (Apis mellifera) worker castes. PLoS ONE 12:e0184108. https://doi.org/10.1371/JOURNAL.PONE.0184108
pubmed: 28877227
pmcid: 5587260
Inoue N, Hanada K, Tsuji N et al (2001) Characterization of phagocytic hemocytes in Ornithodoros moubata (Acari: Ixodidae). J Med Entomol 38:514–519. https://doi.org/10.1603/0022-2585-38.4.514
pubmed: 11476331
Kishi S, Slack BE, Uchiyama J, Zhdanova IV (2009) Zebrafish as a genetic model in biological and behavioral gerontology: where development meets aging in vertebrates—a mini-review. Gerontology 55:430–441. https://doi.org/10.1159/000228892
pubmed: 19654474
pmcid: 2820570
Klass MR (1977) Aging in the nematode Caenorhabditis elegans: major biological and environmental factors influencing life span. Mech Ageing Dev 6:413–429. https://doi.org/10.1016/0047-6374(77)90043-4
pubmed: 926867
Kurtz J (2002) Phagocytosis by invertebrate hemocytes: Causes of individual variation in Panorpa vulgaris scorpionflies. Microsc Res Tech 57:456–468. https://doi.org/10.1002/JEMT.10099
pubmed: 12112428
Lanot R, Zachary D, Holder F, Meister M (2001) Postembryonic hematopoiesis in Drosophila. Dev Biol 230:243–257. https://doi.org/10.1006/dbio.2000.0123
pubmed: 11161576
Laughton AM, Fan MH, Gerardo NM (2014) The combined effects of bacterial symbionts and aging on life history traits in the pea aphid, Acyrthosiphon pisum. Appl Environ Microbiol 80:470–477. https://doi.org/10.1128/AEM.02657-13
pubmed: 24185857
pmcid: 3911086
Lavin Y, Mortha A, Rahman A, Merad M (2015) Regulation of macrophage development and function in peripheral tissues. Nat Rev Immunol 15:731–744. https://doi.org/10.1038/nri3920
pubmed: 26603899
pmcid: 4706379
Lex K, Maia M, Lopes-bastos B et al (2020) Telomere shortening produces an inflammatory environment that increases tumor incidence in zebrafish. Proc Natl Acad Sci 117:15066–15074. https://doi.org/10.1073/pnas.1920049117
pubmed: 32554492
pmcid: 7334448
Li X, Li C, Zhang W et al (2023) Inflammation and aging: signaling pathways and intervention therapies. Signal Transduct Target Ther. https://doi.org/10.1038/s41392-023-01502-8
pubmed: 38155175
pmcid: 10721786
Linehan E, Dombrowski Y, Snoddy R et al (2014) Aging impairs peritoneal but not bone marrow-derived macrophage phagocytosis. Aging Cell 13:699–708. https://doi.org/10.1111/acel.12223
pubmed: 24813244
pmcid: 4326936
Liu T, Liu F, Peng L-W et al (2018) The peritoneal macrophages in inflammatory diseases and abdominal cancers. Oncol Res 26:817–826. https://doi.org/10.3727/096504017X15130753659625
pubmed: 29237519
pmcid: 7844755
Liu S, Zheng S-C, Li Y-L et al (2020) Hemocyte-mediated phagocytosis in crustaceans. Front Immunol 11:523443. https://doi.org/10.3389/fimmu.2020.00268
Lv S, Xu J, Zhao J et al (2014) Classification and phagocytosis of circulating haemocytes in Chinese mitten crab (Eriocheir sinensis) and the effect of extrinsic stimulation on circulating haemocytes in vivo. Fish Shellfish Immunol 39:415–422. https://doi.org/10.1016/j.fsi.2014.05.036
pubmed: 24929244
Mackenzie DK, Bussière LF, Tinsley MC (2011) Senescence of the cellular immune response in Drosophila melanogaster. Exp Gerontol. https://doi.org/10.1016/j.exger.2011.07.004
pubmed: 21798332
Mandujano-Tinoco EA, Sultan E, Ottolenghi A et al (2021) Evolution of cellular immunity effector cells; perspective on cytotoxic and phagocytic cellular lineages. Cells 10:1853. https://doi.org/10.3390/cells10081853
pubmed: 34440622
pmcid: 8394812
McCuskey RS, McCuskey PA (1990) Fine structure and function of Kupffer cells. J Electron Microsc Tech 14:237–246. https://doi.org/10.1002/jemt.1060140305
pubmed: 2338588
Mergan L, Driesschaert B, Temmerman L (2023) Endocytic coelomocytes are required for lifespan extension by axenic dietary restriction. PLoS ONE 18:e0287933. https://doi.org/10.1371/journal.pone.0287933
pubmed: 37368903
pmcid: 10298762
Merkling SH, Lambrechts L (2020) Taking insect immunity to the single-cell level. Trends Immunol 41:190–199. https://doi.org/10.1016/j.it.2020.01.002
pubmed: 32035764
Mogilenko DA, Shpynov O, Andhey PS et al (2021) Comprehensive profiling of an aging immune system reveals clonal GZMK+ CD8+ T cells as conserved hallmark of inflammaging. Immunity 54:99-115.e12. https://doi.org/10.1016/j.immuni.2020.11.005
pubmed: 33271118
Morabito G, Dönertas HM, Sperti L et al (2023) Spontaneous onset of cellular markers of inflammation and genome instability during aging in the immune niche of the naturally short-lived turquoise killifish (Nothobranchius furzeri). bioRxiv. https://doi.org/10.1101/2023.02.06.527346
pubmed: 37546983
pmcid: 10245583
Mosca F, Narcisi V, Cargini D et al (2011) Age related properties of the Adriatic clam Chamelea gallina (L. 1758) hemocytes. Fish Shellfish Immunol 31:1106–1112. https://doi.org/10.1016/j.fsi.2011.09.017
pubmed: 22001736
Murphy CT, McCarroll SA, Bargmann CI et al (2003) Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424:277–283. https://doi.org/10.1038/nature01789
pubmed: 12845331
Musrati MA, De Baetselier P, Movahedi K, Van Ginderachter JA (2023) Ontogeny, functions and reprogramming of Kupffer cells upon infectious disease. Front Immunol 14:1238452. https://doi.org/10.3389/fimmu.2023.1238452
pubmed: 37691953
pmcid: 10485603
Ottaviani E, Franchini A, Barbieri D, Kletsas D (1998) Comparative and morphofunctional studies on Mytilus galloprovincialis hemocytes: presence of two aging-related hemocyte stages. Ital J Zool 65:349–354. https://doi.org/10.1080/11250009809386772
Park J-KK, Park S-KK (2017) Coelomocytes are required for lifespan extension via different methods of dietary restriction in C. elegans. Toxicol Environ Health Sci 9:59–63. https://doi.org/10.1007/s13530-017-0304-6
Park S-K, Link CD, Johnson TE (2010) Life-span extension by dietary restriction is mediated by NLP-7 signaling and coelomocyte endocytosis in C. elegans. FASEB J Off Publ Fed Am Soc fo Exp Biol 24:383–392. https://doi.org/10.1096/fj.09-142984
Park Y, Kim Y, Stanley D (2011) Cellular immunosenescence in adult male crickets, Gryllus assimilis. Arch Insect Biochem Physiol 76:185–194. https://doi.org/10.1002/ARCH.20394
pubmed: 21254201
Partridge L, Deelen J, Slagboom PE (2018) Facing up to the global challenges of ageing. Nature 561:45–56. https://doi.org/10.1038/s41586-018-0457-8
pubmed: 30185958
Podleśny-Drabiniok A, Marcora E, Goate AM (2020) Microglial phagocytosis: a disease-associated process emerging from Alzheimer’s disease genetics. Trends Neurosci 43:965–979. https://doi.org/10.1016/j.tins.2020.10.002.Microglial
pubmed: 33127097
pmcid: 9080913
Prinz M, Priller J (2014) Microglia and brain macrophages in the molecular age: from origin to neuropsychiatric disease. Nat Rev Neurosci 15:300–312. https://doi.org/10.1038/nrn3722
pubmed: 24713688
Qian F, Guo X, Wang X et al (2014) Reduced bioenergetics and toll-like receptor 1 function in human polymorphonuclear leukocytes in aging. Aging 6:131–139. https://doi.org/10.18632/aging.100642
pubmed: 24595889
pmcid: 3969281
Rabinovitch M (1995) Professional and non-professional phagocytes: an introduction. Trends Cell Biol 5:85–87. https://doi.org/10.1016/s0962-8924(00)88955-2
pubmed: 14732160
Rattan SIS (2024) Seven knowledge gaps in modern biogerontology. Biogerontology 25:1–8. https://doi.org/10.1007/s10522-023-10089-0
pubmed: 38206540
Ravaiano SV, Barbosa WF, Campos LA, Martins GF (2018) Variations in circulating hemocytes are affected by age and caste in the stingless bee Melipona quadrifasciata. Sci Nat 105:1–8. https://doi.org/10.1007/S00114-018-1573-X/FIGURES/4
Reuter H, Perner B, Wahl F et al (2022) Aging activates the immune system and alters the regenerative capacity in the zebrafish heart. Cells 11:1–21. https://doi.org/10.3390/cells11030345
Roberts RE, Hallett MB (2019) Neutrophil cell shape change: mechanism and signalling during cell spreading and phagocytosis. Int J Mol Sci 20:1383. https://doi.org/10.3390/ijms20061383
pubmed: 30893856
pmcid: 6471475
Roberts RA, Ganey PE, Ju C et al (2007) Role of the Kupffer cell in mediating hepatic toxicity and carcinogenesis. Toxicol Sci 96:2–15. https://doi.org/10.1093/toxsci/kfl173
pubmed: 17122412
Rolff J (2011) Effects of age and gender on immune function of dragonflies (Odonata, Lestidae) from a wild population. Can J Zool 79:2176–2180
Schmid MR, Brockmann A, Pirk CWW et al (2008) Adult honeybees (Apis mellifera L.) abandon hemocytic, but not phenoloxidase-based immunity. J Insect Physiol 54:439–444. https://doi.org/10.1016/j.jinsphys.2007.11.002
pubmed: 18164310
Shevyrev D, Tereshchenko V, Berezina TN, Rybtsov S (2023) Hematopoietic stem cells and the immune system in development and aging. Int J Mol Sci 24:5862. https://doi.org/10.3390/ijms24065862
pubmed: 36982935
pmcid: 10056303
Söderhäll I (2016) Crustacean hematopoiesis. Dev Comp Immunol 58:129–141. https://doi.org/10.1016/j.dci.2015.12.009
pubmed: 26721583
Stranks AJ, Hansen AL, Panse I et al (2015) Autophagy controls acquisition of aging features in macrophages. J Innate Immun 7:375–391. https://doi.org/10.1159/000370112
pubmed: 25764971
pmcid: 4386145
Sun C, Shao Y, Iqbal J (2023) Insect insights at the single-cell level: technologies and applications. Cells 13:91. https://doi.org/10.3390/cells13010091
pubmed: 38201295
pmcid: 10777908
Tanay A, Sebé-Pedrós A (2021) Evolutionary cell type mapping with single-cell genomics. Trends Genet 37:919–932. https://doi.org/10.1016/j.tig.2021.04.008
pubmed: 34020820
Terman A (2001) Garbage catastrophe theory of aging: imperfect removal of oxidative damage? Redox Rep 6:15–26. https://doi.org/10.1179/135100001101535996
pubmed: 11333111
Uribe-Querol E, Rosales C (2020) Phagocytosis: our current understanding of a universal biological process. Front Immunol 11:1–13. https://doi.org/10.3389/fimmu.2020.01066
Valenzano DR, Benayoun BA, Singh PP et al (2015) The African turquoise killifish genome provides insights into evolution and genetic architecture of lifespan. Cell 163:1539–1554. https://doi.org/10.1016/j.cell.2015.11.008
pubmed: 26638078
pmcid: 4684691
Van Houcke J, Bollaerts I, Geeraerts E et al (2017) Successful optic nerve regeneration in the senescent zebra fish despite age-related decline of cell intrinsic and extrinsic response processes. Neurobiol Aging 60:1–10. https://doi.org/10.1016/j.neurobiolaging.2017.08.013
pubmed: 28917662
Vanhunsel S, Bergmans S, Beckers A et al (2021) The killifish visual system as an in vivo model to study brain aging and rejuvenation. NPJ Aging Mech Dis 7:22. https://doi.org/10.1038/s41514-021-00077-4
pubmed: 34404797
pmcid: 8371010
Vanhunsel S, Bergmans S, Beckers A et al (2022) The age factor in optic nerve regeneration: Intrinsic and extrinsic barriers hinder successful recovery in the short-living killifish. Aging Cell 21:1–24. https://doi.org/10.1111/acel.13537
Videla LA, Tapia G, Fernández V et al (2013) Communications in free radical research influence of aging on Kupffer cell respiratory activity in relation to particle phagocytosis and oxidative stress parameters in mouse liver. Redox Rep 6:155–159. https://doi.org/10.1179/135100001101536265
Vogelweith F, Foitzik S, Meunier J (2017) Age, sex, mating status, but not social isolation interact to shape basal immunity in a group-living insect. J Insect Physiol 103:64–70. https://doi.org/10.1016/J.JINSPHYS.2017.10.007
pubmed: 29038016
Wong CK, Smith CA, Sakamoto K et al (2017) Aging impairs alveolar macrophage phagocytosis and increases influenza-induced mortality in mice. J Immunol 199:1060–1068. https://doi.org/10.4049/jimmunol.1700397
pubmed: 28646038
Wosik J, Suarez-Villagran M, Miller JH et al (2019) Macrophage phenotype bioengineered by magnetic, genetic, or pharmacologic interference. Immunol Res 67:1–11. https://doi.org/10.1007/s12026-019-9066-3
pubmed: 30649660
Zhang Y, Ouyang D, Chen YH, Xia H (2022) Peritoneal resident macrophages in tumor metastasis and immunotherapy. Front Cell Dev Biol 10:948952. https://doi.org/10.3389/fcell.2022.948952
pubmed: 36035994
pmcid: 9402905
Zimmerman SM, Hinkson IV, Elias JE, Kim SK (2015) Reproductive aging drives protein accumulation in the uterus and limits lifespan in C. elegans. PLoS Genet 11:e1005725. https://doi.org/10.1371/journal.pgen.1005725
pubmed: 26656270
pmcid: 4676719