Advertisement

Innate Immunity Under the Exposome of Space Flight

  • Judith-Irina BuchheimEmail author
  • Matthias Feuerecker
  • Alexander Choukér
Chapter

Abstract

Host defense is key to survival of every living organism. The innate immune system, the evolutionarily oldest form of defense against invading pathogens, is present in all life and the result of long years of adaptation to the environment. A fast, less-specific reply to microbial threats using cellular and humoral components without the build-up of an immunological memory are its features. As we progress exploring the universe, manned space missions will become even more frequent and longer in duration. We are striving to explore the possibilities of permanently manned space stations like the International Space Station or the planned “Deep Space Gateway” or just “Gateway” as well as further missions to Earth’s moon and Mars. Astronauts are living and working in a uniquely stressful environment. To ensure safe travel and return, it is our duty to protect them from potential hazards and health threats during their adaptation to this new living environment. The first observations gathered during the Apollo missions made it clear that astronauts become more susceptible to infection. The past years of research have identified various immune alterations. The innate system’s central mechanisms such as the generation of reactive oxygen species, phagocytosis, and regulation of the core body temperature become compromised. Yet little can we explain, and nor can we prevent these changes from happening. Nevertheless, it seems evident that maintaining a well-functioning immune system is the prerequisite for space travel. To further expand our knowledge, more research is necessary. We also need to draw information from terrestrial space analog research such as bed rest studies, parabolic flight campaigns, or Antarctic winter-over. Improving the resources aboard for inflight analyses and encouraging reporting of symptoms and disease will help to develop effective countermeasures.

Notes

Acknowledgments

This work has been supported by the DLR on behalf of the Federal Ministry of Economics and Technology (BMWi 50WB0719 and 50WB0919, 50WB1319), the European Space Agency (ESA’s ELIPS 3 and 4 program, and E3P), the Russian Space Agency (Roscosmos), and the program of fundamental research (theme 65.1) of the Institute for Biomedical Problems (IBMP). We explicitly thank all the helping hands, operators, scientists, and administrators at Roscosmos, IBMP, TsNIIMash in Russia, at ESA, CNES, and DLR as well as the NASA Kennedy Space Centre and the Johnsons’ Space Centre, who made this project possible. Our highest appreciation is expressed to the ISS crews who have participated with motivation and who realized these studies with outstanding professionalism.

In honor and memory of Cosmonaut Dr. Boris Morukov former vice director of IBMP and mission director of Mars500 who passed away in 2015.

References

  1. Allebban Z, Ichiki AT, Gibson LA, Jones JB, Congdon CC, Lange RD (1994) Effects of spaceflight on the number of rat peripheral blood leukocytes and lymphocyte subsets. J Leukoc Biol 55:209–213CrossRefGoogle Scholar
  2. Baqai FP et al (2009) Effects of spaceflight on innate immune function and antioxidant gene expression. J Appl Physiol 106:1935–1942.  https://doi.org/10.1152/japplphysiol.91361.2008CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bascove M, Gueguinou N, Schaerlinger B, Gauquelin-Koch G, Frippiat JP (2011) Decrease in antibody somatic hypermutation frequency under extreme, extended spaceflight conditions. FASEB J 25:2947–2955.  https://doi.org/10.1096/fj.11-185215CrossRefGoogle Scholar
  4. Bauer ME, Fuente Mde L (2016) The role of oxidative and inflammatory stress and persistent viral infections in immunosenescence. Mech Ageing Dev 158:27–37.  https://doi.org/10.1016/j.mad.2016.01.001CrossRefPubMedGoogle Scholar
  5. Benjamin CL et al (2016) Decreases in thymopoiesis of astronauts returning from space flight. JCI Insight 1:e88787.  https://doi.org/10.1172/jci.insight.88787CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bottazzi B, Doni A, Garlanda C, Mantovani A (2010) An integrated view of humoral innate immunity: pentraxins as a paradigm. Annu Rev Immunol 28:157–183.  https://doi.org/10.1146/annurev-immunol-030409-101305CrossRefPubMedGoogle Scholar
  7. Branzk N, Lubojemska A, Hardison SE, Wang Q, Gutierrez MG, Brown GD, Papayannopoulos V (2014) Neutrophils sense microbe size and selectively release neutrophil extracellular traps in response to large pathogens. Nat Immunol 15:1017–1025.  https://doi.org/10.1038/ni.2987CrossRefPubMedPubMedCentralGoogle Scholar
  8. Buchheim J-I et al (2018) Oxidative burst and Dectin-1-triggered phagocytosis affected by norepinephrine and endocannabinoids: implications for fungal clearance under stress. Int Immunol 30:79–89.  https://doi.org/10.1093/intimm/dxy001CrossRefPubMedGoogle Scholar
  9. Buchheim J-I et al (2019) Stress related shift toward inflammaging in cosmonauts after long-duration space flight. Front Physiol 10:85.  https://doi.org/10.3389/fphys.2019.00085CrossRefPubMedPubMedCentralGoogle Scholar
  10. Buscher K, Marcovecchio P, Hedrick CC, Ley K (2017) Patrolling mechanics of non-classical monocytes in vascular inflammation. Front Cardiovasc Med 4:80.  https://doi.org/10.3389/fcvm.2017.00080CrossRefPubMedPubMedCentralGoogle Scholar
  11. Carrion Sde J, Leal SM Jr, Ghannoum MA, Aimanianda V, Latge JP, Pearlman E (2013) The RodA hydrophobin on Aspergillus fumigatus spores masks dectin-1- and dectin-2-dependent responses and enhances fungal survival in vivo. J Immunol 191:2581–2588.  https://doi.org/10.4049/jimmunol.1300748CrossRefPubMedGoogle Scholar
  12. Chouker A et al (2001) Simulated microgravity, psychic stress, and immune cells in men: observations during 120-day 6 degrees HDT. J Appl Physiol 90:1736–1743.  https://doi.org/10.1152/jappl.2001.90.5.1736CrossRefPubMedGoogle Scholar
  13. Chouker A et al (2002) Effects of confinement (110 and 240 days) on neuroendocrine stress response and changes of immune cells in men. J Appl Physiol 92:1619–1627.  https://doi.org/10.1152/japplphysiol.00732.2001CrossRefPubMedGoogle Scholar
  14. Chouker A et al (2010) Motion sickness, stress and the endocannabinoid system. PLoS One 5:e10752.  https://doi.org/10.1371/journal.pone.0010752CrossRefPubMedPubMedCentralGoogle Scholar
  15. Cogoli A (1993) The effect of space flight on human cellular immunity. Environ Med 37:107–116PubMedPubMedCentralGoogle Scholar
  16. Costantini C, Cassatella MA (2011) The defensive alliance between neutrophils and NK cells as a novel arm of innate immunity. J Leukoc Biol 89:221–233.  https://doi.org/10.1189/jlb.0510250CrossRefPubMedGoogle Scholar
  17. Criscitiello MF, de Figueiredo P (2013) Fifty shades of immune defense. PLoS Pathog 9:e1003110.  https://doi.org/10.1371/journal.ppat.1003110CrossRefPubMedPubMedCentralGoogle Scholar
  18. Crucian BE et al (2009) Immune status, latent viral reactivation, and stress during long-duration head-down bed rest. Aviat Space Environ Med 80:A37–A44CrossRefGoogle Scholar
  19. Crucian BE et al (2014) Plasma cytokine concentrations indicate that in vivo hormonal regulation of immunity is altered during long-duration spaceflight. J Interferon Cytokine Res 34:778–786.  https://doi.org/10.1089/jir.2013.0129CrossRefPubMedPubMedCentralGoogle Scholar
  20. Crucian B, Stowe RP, Mehta S, Quiriarte H, Pierson D, Sams C (2015) Alterations in adaptive immunity persist during long-duration spaceflight. NPJ Microgravity 1:15013.  https://doi.org/10.1038/npjmgrav.2015.13CrossRefPubMedPubMedCentralGoogle Scholar
  21. Crucian B, Babiak-Vazquez A, Johnston S, Pierson DL, Ott CM, Sams C (2016a) Incidence of clinical symptoms during long-duration orbital spaceflight. Int J Gen Med 9:383–391.  https://doi.org/10.2147/IJGM.S114188CrossRefPubMedPubMedCentralGoogle Scholar
  22. Crucian B et al (2016b) A case of persistent skin rash and rhinitis with immune system dysregulation onboard the International Space Station. J Allergy Clin Immunol Pract 4:759–762.e758.  https://doi.org/10.1016/j.jaip.2015.12.021CrossRefPubMedPubMedCentralGoogle Scholar
  23. Crucian BE et al (2018) Immune system dysregulation during spaceflight: potential countermeasures for deep space exploration missions. Front Immunol 9:1437.  https://doi.org/10.3389/fimmu.2018.01437CrossRefPubMedPubMedCentralGoogle Scholar
  24. Dhabhar FS (2002) Stress-induced augmentation of immune function—the role of stress hormones, leukocyte trafficking, and cytokines. Brain Behav Immun 16:785–798CrossRefGoogle Scholar
  25. Dhabhar FS, McEwen BS (1997) Acute stress enhances while chronic stress suppresses cell-mediated immunity in vivo: a potential role for leukocyte trafficking. Brain Behav Immun 11:286–306.  https://doi.org/10.1006/brbi.1997.0508CrossRefGoogle Scholar
  26. Feuerecker M et al (2013) Five days of head-down-tilt bed rest induces noninflammatory shedding of L-selectin. J Appl Physiol 115:235–242.  https://doi.org/10.1152/japplphysiol.00381.2013CrossRefPubMedGoogle Scholar
  27. Franceschi C, Bonafe M, Valensin S, Olivieri F, De Luca M, Ottaviani E, De Benedictis G (2000) Inflamm-aging. An evolutionary perspective on immunosenescence. Ann N Y Acad Sci 908:244–254CrossRefGoogle Scholar
  28. Gemignani A et al (2014) How stressful are 105 days of isolation? Sleep EEG patterns and tonic cortisol in healthy volunteers simulating manned flight to Mars. Int J Psychophysiol 93:211–219.  https://doi.org/10.1016/j.ijpsycho.2014.04.008CrossRefGoogle Scholar
  29. Gmunder FK, Konstantinova I, Cogoli A, Lesnyak A, Bogomolov W, Grachov AW (1994) Cellular immunity in cosmonauts during long duration spaceflight on board the orbital MIR station. Aviat Space Environ Med 65:419–423PubMedPubMedCentralGoogle Scholar
  30. Gridley DS et al (2009) Spaceflight effects on T lymphocyte distribution, function and gene expression. J Appl Physiol 106:194–202.  https://doi.org/10.1152/japplphysiol.91126.2008CrossRefGoogle Scholar
  31. Groot Kormelink T, Mol S, de Jong EC, Wauben MHM (2018) The role of extracellular vesicles when innate meets adaptive. Semin Immunopathol.  https://doi.org/10.1007/s00281-018-0681-1
  32. Gueguinou N, Huin-Schohn C, Bascove M, Bueb JL, Tschirhart E, Legrand-Frossi C, Frippiat JP (2009) Could spaceflight-associated immune system weakening preclude the expansion of human presence beyond Earth’s orbit? J Leukoc Biol 86:1027–1038.  https://doi.org/10.1189/jlb.0309167CrossRefGoogle Scholar
  33. Heesterbeek DAC, Angelier ML, Harrison RA, Rooijakkers SHM (2018) Complement and bacterial infections: from molecular mechanisms to therapeutic applications. J Innate Immun 10:455–464.  https://doi.org/10.1159/000491439CrossRefPubMedPubMedCentralGoogle Scholar
  34. Hill MN, Karatsoreos IN, Hillard CJ, McEwen BS (2010) Rapid elevations in limbic endocannabinoid content by glucocorticoid hormones in vivo. Psychoneuroendocrinology 35:1333–1338.  https://doi.org/10.1016/j.psyneuen.2010.03.005CrossRefPubMedPubMedCentralGoogle Scholar
  35. Hopke A, Nicke N, Hidu EE, Degani G, Popolo L, Wheeler RT (2016) Neutrophil attack triggers extracellular trap-dependent Candida cell wall remodeling and altered immune recognition. PLoS Pathog 12:e1005644.  https://doi.org/10.1371/journal.ppat.1005644CrossRefPubMedPubMedCentralGoogle Scholar
  36. Jacubowski A et al (2015) The impact of long-term confinement and exercise on central and peripheral stress markers. Physiol Behav 152:106–111.  https://doi.org/10.1016/j.physbeh.2015.09.017CrossRefGoogle Scholar
  37. Johnston RS, Dietlein LF, Berry CA (1975a) Biomedical results of Apollo. Nasa Sp 368. Scientific and Technical Information Office, National Aeronautics and Space Administration: for sale by the Supt. of Docs., U.S. Govt. Printing Office, Washington, DCGoogle Scholar
  38. Johnston RS, Dietlein LF, Charles AB (1975b) Biomedical results of Apollo. NASA, Washington, DCGoogle Scholar
  39. Jurberg AD, Cotta-de-Almeida V, Temerozo JR, Savino W, Bou-Habib DC, Riederer I (2018) Neuroendocrine control of macrophage development and function. Front Immunol 9:1440.  https://doi.org/10.3389/fimmu.2018.01440CrossRefPubMedPubMedCentralGoogle Scholar
  40. Kaufmann I, Schachtner T, Feuerecker M, Schelling G, Thiel M, Chouker A (2009) Parabolic flight primes cytotoxic capabilities of polymorphonuclear leucocytes in humans. Eur J Clin Investig 39:723–728.  https://doi.org/10.1111/j.1365-2362.2009.02136.xCrossRefGoogle Scholar
  41. Kaufmann I, Feuerecker M, Salam A, Schelling G, Thiel M, Chouker A (2011) Adenosine A2(A) receptor modulates the oxidative stress response of primed polymorphonuclear leukocytes after parabolic flight. Hum Immunol 72:547–552.  https://doi.org/10.1016/j.humimm.2011.03.021CrossRefGoogle Scholar
  42. Kaur I, Simons ER, Castro VA, Mark Ott C, Pierson DL (2004) Changes in neutrophil functions in astronauts. Brain Behav Immun 18:443–450.  https://doi.org/10.1016/j.bbi.2003.10.005CrossRefPubMedPubMedCentralGoogle Scholar
  43. Kaur I, Simons ER, Castro VA, Ott CM, Pierson DL (2005) Changes in monocyte functions of astronauts. Brain Behav Immun 19:547–554.  https://doi.org/10.1016/j.bbi.2004.12.006CrossRefPubMedPubMedCentralGoogle Scholar
  44. Kaur I, Simons ER, Kapadia AS, Ott CM, Pierson DL (2008) Effect of spaceflight on ability of monocytes to respond to endotoxins of gram-negative bacteria. Clin Vaccine Immunol 15:1523–1528.  https://doi.org/10.1128/CVI.00065-08CrossRefPubMedPubMedCentralGoogle Scholar
  45. Kesimer M et al (2009) Characterization of exosome-like vesicles released from human tracheobronchial ciliated epithelium: a possible role in innate defense. FASEB J 23:1858–1868.  https://doi.org/10.1096/fj.08-119131CrossRefPubMedPubMedCentralGoogle Scholar
  46. Knox BP et al (2016) Characterization of Aspergillus fumigatus isolates from air and surfaces of the International Space Station. mSphere 1.  https://doi.org/10.1128/mSphere.00227-16
  47. Konstantinova IV, Rykova MP, Lesnyak AT, Antropova EA (1993) Immune changes during long-duration missions. J Leukoc Biol 54:189–201CrossRefGoogle Scholar
  48. Kouwaki T, Okamoto M, Tsukamoto H, Fukushima Y, Oshiumi H (2017) Extracellular vesicles deliver host and virus RNA and regulate innate immune response. Int J Mol Sci 18.  https://doi.org/10.3390/ijms18030666
  49. Kumar V, Sharma A (2010) Neutrophils: Cinderella of innate immune system. Int Immunopharmacol 10:1325–1334.  https://doi.org/10.1016/j.intimp.2010.08.012CrossRefPubMedGoogle Scholar
  50. Kvell K, Cooper EL, Engelmann P, Bovari J, Nemeth P (2007) Blurring borders: innate immunity with adaptive features. Clin Dev Immunol 2007:83671.  https://doi.org/10.1155/2007/83671CrossRefPubMedPubMedCentralGoogle Scholar
  51. Mantovani A, Cassatella MA, Costantini C, Jaillon S (2011) Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol 11:519–531.  https://doi.org/10.1038/nri3024CrossRefPubMedGoogle Scholar
  52. Marki A, Esko JD, Pries AR, Ley K (2015) Role of the endothelial surface layer in neutrophil recruitment. J Leukoc Biol 98:503–515.  https://doi.org/10.1189/jlb.3MR0115-011RCrossRefPubMedPubMedCentralGoogle Scholar
  53. Marucha PT, Kiecolt-Glaser JK, Favagehi M (1998) Mucosal wound healing is impaired by examination stress. Psychosom Med 60:362–365CrossRefGoogle Scholar
  54. Mehta SK, Crucian B, Pierson DL, Sams C, Stowe RP (2007) Monitoring immune system function and reactivation of latent viruses in the Artificial Gravity Pilot Study. J Gravit Physiol 14:P21–P25PubMedGoogle Scholar
  55. Mehta SK, Laudenslager ML, Stowe RP, Crucian BE, Feiveson AH, Sams CF, Pierson DL (2017a) Latent virus reactivation in astronauts on the international space station. NPJ Microgravity 3:11.  https://doi.org/10.1038/s41526-017-0015-yCrossRefPubMedPubMedCentralGoogle Scholar
  56. Mehta SK et al (2017b) Localization of VZV in saliva of zoster patients. J Med Virol 89:1686–1689.  https://doi.org/10.1002/jmv.24807CrossRefPubMedGoogle Scholar
  57. Michel EL, Johnston RS, Dietlein LF (1976) Biomedical results of the Skylab Program. Life Sci Space Res 14:3–18PubMedGoogle Scholar
  58. Murphy K, Travers P, Walport M, Janeway C (2012) Janeway’s immunobiology, 8th edn. Garland Science, New YorkGoogle Scholar
  59. Novikova N et al (2006) Survey of environmental biocontamination on board the International Space Station. Res Microbiol 157:5–12.  https://doi.org/10.1016/j.resmic.2005.07.010CrossRefPubMedGoogle Scholar
  60. Nussler AK, Wittel UA, Nussler NC, Beger HG (1999) Leukocytes, the Janus cells in inflammatory disease. Langenbeck’s Arch Surg 384:222–232CrossRefGoogle Scholar
  61. Pagel JI, Chouker A (2016) Effects of isolation and confinement on humans-implications for manned space explorations. J Appl Physiol 120:1449–1457.  https://doi.org/10.1152/japplphysiol.00928.2015CrossRefPubMedPubMedCentralGoogle Scholar
  62. Paulsen K et al (2015) Regulation of ICAM-1 in cells of the monocyte/macrophage system in microgravity. Biomed Res Int 2015:538786.  https://doi.org/10.1155/2015/538786CrossRefGoogle Scholar
  63. Pawelec G, Gouttefangeas C (2006) T-cell dysregulation caused by chronic antigenic stress: the role of CMV in immunosenescence? Aging Clin Exp Res 18:171–173CrossRefGoogle Scholar
  64. Pecaut MJ et al (2003) Genetic models in applied physiology: selected contribution: effects of spaceflight on immunity in the C57BL/6 mouse. I. Immune population distributions. J Appl Physiol 94:2085–2094.  https://doi.org/10.1152/japplphysiol.01052.2002CrossRefGoogle Scholar
  65. Romsdahl J et al (2018) Characterization of Aspergillus niger Isolated from the International Space Station. mSystems 3.  https://doi.org/10.1128/mSystems.00112-18
  66. Rot A, von Andrian UH (2004) Chemokines in innate and adaptive host defense: basic chemokinese grammar for immune cells. Annu Rev Immunol 22:891–928.  https://doi.org/10.1146/annurev.immunol.22.012703.104543CrossRefPubMedPubMedCentralGoogle Scholar
  67. Roth S et al (2016) Vav proteins are key regulators of Card9 signaling for innate antifungal immunity. Cell Rep 17:2572–2583.  https://doi.org/10.1016/j.celrep.2016.11.018CrossRefPubMedPubMedCentralGoogle Scholar
  68. Salvi V et al (2018) Exosome-delivered microRNAs promote IFN-alpha secretion by human plasmacytoid DCs via TLR7. JCI Insight 3.  https://doi.org/10.1172/jci.insight.98204
  69. Sanada F, Taniyama Y, Muratsu J, Otsu R, Shimizu H, Rakugi H, Morishita R (2018) Source of chronic inflammation in aging. Front Cardiovasc Med 5:12.  https://doi.org/10.3389/fcvm.2018.00012CrossRefPubMedPubMedCentralGoogle Scholar
  70. Scapini P, Bazzoni F, Cassatella MA (2008) Regulation of B-cell-activating factor (BAFF)/B lymphocyte stimulator (BLyS) expression in human neutrophils. Immunol Lett 116:1–6.  https://doi.org/10.1016/j.imlet.2007.11.009CrossRefPubMedGoogle Scholar
  71. Shearer WT et al (2009) Immune responses in adult female volunteers during the bed-rest model of spaceflight: antibodies and cytokines. J Allergy Clin Immunol 123:900–905.  https://doi.org/10.1016/j.jaci.2008.12.016CrossRefPubMedGoogle Scholar
  72. Sitkovsky MV et al (2004) Physiological control of immune response and inflammatory tissue damage by hypoxia-inducible factors and adenosine A2A receptors. Annu Rev Immunol 22:657–682.  https://doi.org/10.1146/annurev.immunol.22.012703.104731CrossRefPubMedGoogle Scholar
  73. Sonnenfeld G (1994) Effect of space flight on cytokine production. Acta Astronaut 33:143–147CrossRefGoogle Scholar
  74. Sorrells SF, Sapolsky RM (2007) An inflammatory review of glucocorticoid actions in the CNS. Brain Behav Immun 21:259–272.  https://doi.org/10.1016/j.bbi.2006.11.006CrossRefPubMedGoogle Scholar
  75. Stahn AC et al (2017) Increased core body temperature in astronauts during long-duration space missions. Sci Rep 7:16180.  https://doi.org/10.1038/s41598-017-15560-wCrossRefPubMedPubMedCentralGoogle Scholar
  76. Stowe RP, Sams CF, Mehta SK, Kaur I, Jones ML, Feeback DL, Pierson DL (1999) Leukocyte subsets and neutrophil function after short-term spaceflight. J Leukoc Biol 65:179–186CrossRefGoogle Scholar
  77. Stowe RP, Mehta SK, Ferrando AA, Feeback DL, Pierson DL (2001) Immune responses and latent herpesvirus reactivation in spaceflight. Aviat Space Environ Med 72:884–891PubMedPubMedCentralGoogle Scholar
  78. Stowe RP, Yetman DL, Storm WF, Sams CF, Pierson DL (2008) Neuroendocrine and immune responses to 16-day bed rest with realistic launch and landing G profiles. Aviat Space Environ Med 79:117–122CrossRefGoogle Scholar
  79. Strewe C et al (2012) Effects of parabolic flight and spaceflight on the endocannabinoid system in humans. Rev Neurosci 23:673–680.  https://doi.org/10.1515/revneuro-2012-0057CrossRefPubMedPubMedCentralGoogle Scholar
  80. Strewe C et al (2015) Functional changes in neutrophils and psychoneuroendocrine responses during 105 days of confinement. J Appl Physiol 118:1122–1127.  https://doi.org/10.1152/japplphysiol.00755.2014CrossRefPubMedGoogle Scholar
  81. Strewe C et al (2018) PlanHab study: consequences of combined normobaric hypoxia and bed rest on adenosine kinetics. Sci Rep 8:1762.  https://doi.org/10.1038/s41598-018-20045-5CrossRefPubMedPubMedCentralGoogle Scholar
  82. Taylor GR, Neale LS, Dardano JR (1986) Immunological analyses of U.S. Space Shuttle crewmembers. Aviat Space Environ Med 57:213–217Google Scholar
  83. Taylor K et al (2014) Toll mediated infection response is altered by gravity and spaceflight in Drosophila. PLoS One 9:e86485.  https://doi.org/10.1371/journal.pone.0086485CrossRefPubMedPubMedCentralGoogle Scholar
  84. Ward C, Rettig TA, Hlavacek S, Bye BA, Pecaut MJ, Chapes SK (2018) Effects of spaceflight on the immunoglobulin repertoire of unimmunized C57BL/6 mice. Life Sci Space Res 16:63–75.  https://doi.org/10.1016/j.lssr.2017.11.003CrossRefGoogle Scholar
  85. West EE, Kolev M, Kemper C (2018) Complement and the regulation of T cell responses. Annu Rev Immunol 36:309–338.  https://doi.org/10.1146/annurev-immunol-042617-053245CrossRefPubMedGoogle Scholar
  86. Wild CP (2012) The exposome: from concept to utility. Int J Epidemiol 41:24–32.  https://doi.org/10.1093/ije/dyr236CrossRefGoogle Scholar
  87. Yeager MP, Pioli PA, Collins J, Barr F, Metzler S, Sites BD, Guyre PM (2016) Glucocorticoids enhance the in vivo migratory response of human monocytes. Brain Behav Immun 54:86–94.  https://doi.org/10.1016/j.bbi.2016.01.004CrossRefPubMedPubMedCentralGoogle Scholar
  88. Yi B et al (2014) 520-d Isolation and confinement simulating a flight to Mars reveals heightened immune responses and alterations of leukocyte phenotype. Brain Behav Immun 40:203–210.  https://doi.org/10.1016/j.bbi.2014.03.018CrossRefGoogle Scholar
  89. Yi B et al (2015) The impact of chronic stress burden of 520-d isolation and confinement on the physiological response to subsequent acute stress challenge. Behav Brain Res 281:111–115.  https://doi.org/10.1016/j.bbr.2014.12.011CrossRefPubMedPubMedCentralGoogle Scholar
  90. Zarbock A, Ley K (2009) Neutrophil adhesion and activation under flow. Microcirculation 16:31–42.  https://doi.org/10.1080/10739680802350104CrossRefPubMedPubMedCentralGoogle Scholar
  91. Zhang Q et al (2010) Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 464:104–107.  https://doi.org/10.1038/nature08780CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Judith-Irina Buchheim
    • 1
    Email author
  • Matthias Feuerecker
    • 1
  • Alexander Choukér
    • 1
  1. 1.Laboratory of Translational Research Stress and Immunity, Department of AnaesthesiologyHospital of the University of Munich (LMU)MunichGermany

Personalised recommendations