Terrestrial stress analogs for spaceflight associated immune system dysregulation

Brain, Behavior, and Immunity

Volumn 39, Issue , 2014, Pages 23-32

  Crucian, Brian ^a   Simpson, Richard J ^b   Mehta, Satish ^c   Stowe, Raymond ^d   Chouker, Alexander ^e   Hwang, Shen An ^f   Actor, Jeffrey K ^f   Salam, Alex P ^g   Pierson, Duane ^a   Sams, Clarence ^a  

^a NASA JOHNSON SPACE CENTER   (United States)

^b UNIVERSITY OF HOUSTON   (United States)

^c EASI   (United States)

^d Microgen Laboratories Inc   (United States)

^e LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^f UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^g CHELSEA AND WESTMINSTER HOSPITAL   (United Kingdom)

Author keywords

Cytokines; Exercise; Immunity; Spaceflight; Stress; T cells

Indexed keywords

ALPHA INTERFERON; CORTICOTROPIN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 8; STRESS HORMONE; TUMOR NECROSIS FACTOR ALPHA;

ACUTE STRESS; ANTARCTICA; ANTIBODY PRODUCTION; ARCTIC; BED REST; BIOREACTOR; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL CULTURE; CELLULAR IMMUNITY; CHRONIC STRESS; CIRCADIAN RHYTHM; COSMONAUT; CYTOKINE PRODUCTION; DISEASE DURATION; EMERGENCY HEALTH SERVICE; EOSINOPHIL; GENE EXPRESSION; HUMAN; HUMORAL IMMUNITY; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMOBILIZATION; IMMUNE DYSREGULATION; KLEBSIELLA PNEUMONIAE INFECTION; LATENT VIRUS INFECTION; LISTERIOSIS; MENTAL STRESS; MICROGRAVITY; MONOCYTE; NEUTROPHIL; NONHUMAN; PHYSICAL STRESS; PHYSIOLOGICAL STRESS; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; RADIATION EXPOSURE; REVIEW; ROTAVIRUS INFECTION; SPACE; SPACE FLIGHT; STRESS; TERRESTRIAL STRESS; VIRUS REACTIVATION; ADAPTATION; CHRONIC DISEASE; IMMUNE SYSTEM; IMMUNOLOGY;

ADAPTATION, PHYSIOLOGICAL; CHRONIC DISEASE; HUMANS; IMMUNE SYSTEM; SPACE FLIGHT; SPACE SIMULATION; STRESS, PHYSIOLOGICAL; STRESS, PSYCHOLOGICAL;

EID: 84902331182     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2014.01.011     Document Type: Review

References (83)

1. Assenmacher I., Mekaouche M., Maurel D., Barbanel G., Givalois L., Boissin J., Malaval F., Ixart G. Chronic orthostatic and antiorthostatic restraint induce neuroendocrine, immune and neurophysiologial disorders in rats. Acta Astronaut. 1995, 36(8-12):545-558.
2. Aviles H., Belay T., Fountain K., Vance M., Sonnenfeld G. Increased susceptibility to Pseudomonas aeruginosa infection under hindlimb-unloading conditions. J. Appl. Physiol. 2003, 95:73.
3. Aviles H., Belay T., Fountain K., Vance M., Sun B., Sonnenfeld G. Active hexose correlated compound enhances resistance to Klebsiella pneumoniae infection in mice in the hindlimb-unloading model of spaceflight conditions. J. Appl. Physiol. 2003, 95:491.
4. Aviles H., Belay T., Vance M., Sun B., Sonnenfeld G. Active hexose correlated compound enhances the immune function of mice in the hindlimb-unloading model of spaceflight conditions. J. Appl. Physiol. 2004, 97:1437.
5. Baker W., Schneider B.A., Kulkarni A., Sloan G., Schaub R., Sypek J., Cannon J.G. P-selectin inhibition suppresses muscle regeneration following injury. J. Leukoc. Biol. 2004, 76:352.
6. Belay T., Aviles H., Vance M., Fountain K., Sonnenfeld G. Effects of the hindlimb-unloading model of spaceflight conditions on resistance of mice to infection with Klebsiella pneumoniae. J. Allergy Clin. Immunol. 2002, 110:262.
7. Blaber E., Marcal H., Burns B.P. Bioastronautics: the influence of microgravity on astronaut health. Astrobiology 2010, 10:463.
8. Blutt S.E., Conner M.E. Kinetics of rotavirus infection in mice are not altered in a ground-based model of spaceflight. Aviat. Space Environ. Med. 2004, 75:215.
9. Boonyaratanakornkit J.B., Cogoli A., Li C.F., Schopper T., Pippia P., Galleri G., Meloni M.A., Hughes-Fulford M. Key gravity-sensitive signaling pathways drive T cell activation. FASEB J. 2005, 19:2020.
10. Buravkova L.B., Rykova M.P., Grigorieva V., Antropova E.N. Cell interactions in microgravity: cytotoxic effects of natural killer cells in vitro. J. Gravit. Physiol. 2004, 11:P177.
11. Chapes S.K., Morrison D.R., Guikema J.A., Lewis M.L., Spooner B.S. Production and action of cytokines in space. Adv. Space Res. 1994, 14:5.
12. Chouker A., Thiel M., Baranov V., Meshkov D., Kotov A., Peter K., Messmer K., Christ F. Simulated microgravity, psychic stress, and immune cells in men: observations during 120-day 6 degrees HDT. J. Appl. Physiol. 2001, 90:1736.
13. Cogoli A., Bechler B., Cogoli-Greuter M., Criswell S.B., Joller H., Joller P., Hunzinger E., Muller O. Mitogenic signal transduction in T lymphocytes in microgravity. J. Leukoc. Biol. 1993, 53:569.
14. Cogoli A., Cogoli-Greuter M. Activation and proliferation of lymphocytes and other mammalian cells in microgravity. Adv. Space Biol. Med. 1997, 6:33.
15. Crucian, B., Sams, C., 2004. Alterations in immune function during a high-fidelity 14-day undersea spaceflight mission simulation - the NASA NEEMO project. In: 75th Annual Meeting of the Aerospace Medical Association.
16. Crucian B., Lee P., Stowe R., Jones J., Effenhauser R., Widen R., Sams C. Immune system changes during simulated planetary exploration on Devon Island, high arctic. BMC Immunol. 2007, 8:7.
17. Crucian B.E., Stowe R.P., Pierson D.L., Sams C.F. Immune system dysregulation following short- vs long-duration spaceflight. Aviat. Space Environ. Med. 2008, 79:835.
18. Crucian B.E., Stowe R.P., Mehta S.K., Yetman D.L., Leal M.J., Quiriarte H.D., Pierson D.L., Sams C.F. Immune status, latent viral reactivation, and stress during long-duration head-down bed rest. Aviat. Space Environ. Med. 2009, 80:A37.
19. Crucian B., Feuerecker M., Salam A., Rybka A., Stowe R., Morrels M., Mehta S., Quiriarte H., Quintens R., Thieme U., Kaufmann I., Baatout D., Pierson D., Sams C., Chouker A. Immune system dysregulation and latent herpesvirus reactivation during winterover at Concordia Station, Dome C, Antarctica 2012, NASA Human Research Program, Investigators Working Group Meeting, Houston, TX.
20. Crucian B., Stowe R., Mehta S., Uchakin P., Quiriarte H., Pierson D., Sams C. Immune system dysregulation occurs during short duration spaceflight on board the space shuttle. J. Clin. Immunol. 2013, 33(2):456-465.
21. Crucian B., Zwart S., Mehta S., Stowe R., Uchakin P., Quiriarte H., Pierson D., Smith S.M., Sams C. Immune system dysregulation persists during long-duration spaceflight 2013, AAAAI Annual Meeting, San Antonio, TX.
22. Dhabhar F.S. Enhancing versus suppressive effects of stress on immune function: implications for immunoprotection and immunopathology. NeuroImmunoModulation 2009, 16:300.
23. Eskandari F., Sternberg E.M. Neural-immune interactions in health and disease. Ann. N. Y. Acad. Sci. 2002, 966:20.
24. Felix K., Wise K., Manna S., Yamauchi K., Wilson B.L., Thomas R.L., Kulkarni A., Pellis N.R., Ramesh G.T. Altered cytokine expression in tissues of mice subjected to simulated microgravity. Mol. Cell. Biochem. 2004, 266:79.
25. Feuerecker, M., Crucian, B., Salam, A., Schmitt, D., Stowe, R., Morrels, M., Mehta, S., Strewe, C., Martignoni, A., Quintens, R., Kaufmann, I., Schelling, G., Baatout, S., Abbal, M., Thiel, M., Pierson, D., Sams, C., Chouker, A., 2012. Consequences of longterm Confinement and Hypobaric Hypoxia on Immunity in the Antarctic-Concordia Environment (CHOICE): a hypoxia controlled field study to prepare for manned exploration class mission. In: Life in Space for Life on Earth - 12th European Life Sciences Symposium 33rd Annual International Gravitational Physiology Meeting, vol. June 18-22, Aberdeen, United Kingdom.
26. Fitzgerald W., Chen S., Walz C., Zimmerberg J., Margolis L., Grivel J.C. Immune suppression of human lymphoid tissues and cells in rotating suspension culture and onboard the International Space Station. In Vitro Cell. Dev. Biol. Anim. 2009, 45:622.
27. Glaser R., Kiecolt-Glaser J.K., Speicher C.E., Holliday J.E. Stress, loneliness, and changes in herpesvirus latency. J. Behav. Med. 1985, 8:249.
28. Glaser R., Friedman S.B., Smyth J., Ader R., Bijur P., Brunell P., Cohen N., Krilov L.R., Lifrak S.T., Stone A., Toffler P. The differential impact of training stress and final examination stress on herpesvirus latency at the United States Military Academy at West Point. Brain Behav. Immun. 1999, 13:240.
29. Gleeson M., Pyne D.B., Austin J.P., Lynn Francis J., Clancy R.L., McDonald W.A., Fricker P.A. Epstein-Barr virus reactivation and upper-respiratory illness in elite swimmers. Med. Sci. Sports Exerc. 2002, 34:411.
30. Gmunder F.K., Baisch F., Bechler B., Cogoli A., Cogoli M., Joller P.W., Maass H., Muller J., Ziegler W.H. Effect of head-down tilt bed rest (10 days) on lymphocyte reactivity. Acta Physiol. Scand. Suppl. 1992, 604:131.
31. Gueguinou N., Huin-Schohn C., Bascove M., Bueb J.L., Tschirhart E., Legrand-Frossi C., Frippiat J.P. Could spaceflight-associated immune system weakening preclude the expansion of human presence beyond Earth's orbit?. J. Leukoc. Biol. 2009, 86:1027.
32. Hales N.W., Yamauchi K., Alicea A., Sundaresan A., Pellis N.R., Kulkarni A.D. A countermeasure to ameliorate immune dysfunction in in vitro simulated microgravity environment: role of cellularnucleotide nutrition. In Vitro Cell. Dev. Biol. Anim. 2002, 38:213.
33. Hargens A.R., Mortensen W.W., Gershuni D.H., Crenshaw A.G., Lieber R.L., Akeson W.H. Long-term measurement of muscle function in the dog hindlimb using a new apparatus. J. Orthop. Res. 1984, 1:284.
34. Hashemi B.B., Penkala J.E., Vens C., Huls H., Cubbage M., Sams C.F. T cell activation responses are differentially regulated during clinorotation and in spaceflight. FASEB J. 1999, 13:2071.
35. Hughes-Fulford M. Changes in gene expression and signal transduction in microgravity. J. Gravit. Physiol. 2001, 8:P1.
36. Hughes-Fulford M. Function of the cytoskeleton in gravisensing during spaceflight. Adv. Space Res. 2003, 32:1585.
37. Ilcus, L.S., Johnston, S.L., Moynihan, S., Kerstman, E.L., Marshall, G.D., 2009. Rashes and exanthems on long duration space flights. In: Annual Meeting of the Aerospace Medical Association, Los Angeles, CA.
38. Jung C.K., Chung S., Lee Y.Y., Hwang S.H., Kang C.S., Lee K.Y. Monocyte adhesion to endothelial cells increases with hind-limb unloading in rats. Aviat. Space Environ. Med. 2005, 76:720.
39. Kulkarni A.D., Yamauchi K., Sundaresan A., Ramesh G.T., Pellis N.R. Countermeasure for space flight effects on immune system: nutritional nucleotides. Gravit. Space Biol. Bull. 2005, 18:101.
40. Lebsack T.W., Kreulen C., Deever D.B., Harris D.T., Witten M.L. Substance P effects on developing thymocytes in hindlimb unloaded rats. Aviat. Space Environ. Med. 2005, 76:11.
41. Lee E.H., Ding W., Kulkarni A.D., Granstein R.D. Tumor growth and immune function in mice during hind-limb unloading. Aviat. Space Environ. Med. 2005, 76:536.
42. Licato L.L., Grimm E.A. Multiple interleukin-2 signaling pathways differentially regulated by microgravity. Immunopharmacology 1999, 44:273.
43. Mallis M.M., DeRoshia C.W. Circadian rhythms, sleep, and performance in space. Aviat. Space Environ. Med. 2005, 76:B94.
44. Meck J.V., Dreyer S.A., Warren L.E. Long-duration head-down bed rest: project overview, vital signs, and fluid balance. Aviat. Space Environ. Med. 2009, 80:A1.
45. Mehta S.K., Pierson D.L., Cooley H., Dubow R., Lugg D. Epstein-Barr virus reactivation associated with diminished cell-mediated immunity in antarctic expeditioners. J. Med. Virol. 2000, 61:235.
46. Mehta S.K., Stowe R.P., Feiveson A.H., Tyring S.K., Pierson D.L. Reactivation and shedding of cytomegalovirus in astronauts during spaceflight. J. Infect. Dis. 2000, 182:1761.
47. Mehta S.K., Cohrs R.J., Forghani B., Zerbe G., Gilden D.H., Pierson D.L. Stress-induced subclinical reactivation of varicella zoster virus in astronauts. J. Med. Virol. 2004, 72:174.
48. Mehta S.K., Crucian B.E., Stowe R.P., Simpson R.J., Ott C.M., Sams C.F., Pierson D.L. Reactivation of latent viruses is associated with increased plasma cytokines in astronauts. Cytokine 2012, 61:205.
49. Mehta, S., Crucian, B., Stowe, R. Sams, C. Castro, V.A., Ott, C.M., Pierson, D. 2013. Viral reactivation in the International Space Station Crew. NASA Human Research Program, Investigators Working Group Meeting.
50. Mermel L.A. Infection prevention and control during prolonged human space travel. Clin. Infect. Dis. 2013, 56:123.
51. Miller E.S., Sonnenfeld G. Influence of suspension on the expression of protective immunological memory to murine Listeria monocytogenes infection. J. Leukoc. Biol. 1993, 54:578.
52. Miller E.S., Sonnenfeld G. Influence of antiorthostatic suspension on resistance to murine Listeria monocytogenes infection. J. Leukoc. Biol. 1994, 55:371.
53. Morey-Holton E.R., Globus R.K. Hindlimb unloading rodent model: technical aspects. J. Appl. Physiol. 2002, 92:1367.
54. Morey-Holton E., Globus R.K., Kaplansky A., Durnova G. The hindlimb unloading rat model: literature overview, technique update and comparison with space flight data. Adv. Space Biol. Med. 2005, 10:7.
55. O'Donnell P.M., Orshal J.M., Sen D., Sonnenfeld G., Aviles H.O. Effects of exposure of mice to hindlimb unloading on leukocyte subsets and sympathetic nervous system activity. Stress 2009, 12:82.
56. Palinkas L.A., Gunderson E.K., Johnson J.C., Holland A.W. Behavior and performance on long-duration spaceflights: evidence from analogue environments. Aviat. Space Environ. Med. 2000, 71:A29.
57. Payne D.A., Mehta S.K., Tyring S.K., Stowe R.P., Pierson D.L. Incidence of Epstein-Barr virus in astronaut saliva during spaceflight. Aviat. Space Environ. Med. 1999, 70:1211.
58. Pellis N.R., Goodwin T.J., Risin D., McIntyre B.W., Pizzini R.P., Cooper D., Baker T.L., Spaulding G.F. Changes in gravity inhibit lymphocyte locomotion through type I collagen. In Vitro Cell. Dev. Biol. Anim. 1997, 33:398.
59. Pierson D.L., Stowe R.P., Phillips T.M., Lugg D.J., Mehta S.K. Epstein-Barr virus shedding by astronauts during space flight. Brain Behav. Immun. 2005, 19:235.
60. Rivera C.A., Tcharmtchi M.H., Mendoza L., Smith C.W. Endotoxemia and hepatic injury in a rodent model of hindlimb unloading. J. Appl. Physiol. 2003, 95:1656.
61. Ruger, M., Crucian, B., Mehta, S. Pierson, D. Sams, C., Scheer, F.A.J.L., Butler, M., Barger, L. Lockley, S., Shea, S.A., 2013. Preliminary results on the effects of sleep deprivation and circadian misalignment on immunological markers in habitually active participants. In: 27th Annual Meeting of the APSS (SLEEP 2013), Baltimore, MD.
62. Salam A. Exploration class mission on Earth: lessons learnt from life in extreme Antarctic Isolation and confinement. Stress Challenges and Immunity in Space 2012, Springer, pp. 425-439.
63. Sarid O., Anson O., Yaari A., Margalith M. Epstein-Barr virus specific salivary antibodies as related to stress caused by examinations. J. Med. Virol. 2001, 64:149.
64. Sarkar P., Sarkar S., Ramesh V., Kim H., Barnes S., Kulkarni A., Hall J.C., Wilson B.L., Thomas R.L., Pellis N.R., Ramesh G.T. Proteomic analysis of mouse hypothalamus under simulated microgravity. Neurochem. Res. 2008, 33:2335.
65. Schmitt D.A., Schaffar L., Taylor G.R., Loftin K.C., Schneider V.S., Koebel A., Abbal M., Sonnenfeld G., Lewis D.E., Reuben J.R., Ferebee R. Use of bed rest and head-down tilt to simulate spaceflight-induce immune system changes. J. Interferon Cytokine Res. 1996, 16:151.
66. Schmitt D.A., Schwarzenberg M., Tkaczuk J., Hebrard S., Brandenberger G., Mauco G., Cogoli-Greuter M., Abbal M. Head-down tilt bed rest and immune responses. Pflugers Arch. 2000, 441:R79.
67. Shearer W.T., Lugg D.J., Rosenblatt H.M., Nickolls P.M., Sharp R.M., Reuben J.M., Ochs H.D. Antibody responses to bacteriophage phi X-174 in human subjects exposed to the antarctic winter-over model of spaceflight. J. Allergy Clin. Immunol. 2001, 107:160.
68. Simpson R.J., Florida-James G.D., Cosgrove C., Whyte G.P., Macrae S., Pircher H., Guy K. High-intensity exercise elicits the mobilization of senescent T lymphocytes into the peripheral blood compartment in human subjects. J. Appl. Physiol. 2007, 103:396.
69. Simpson R.J., Cosgrove C., Chee M.M., McFarlin B.K., Bartlett D.B., Spielmann G., O'Connor D.P., Pircher H., Shiels P.G. Senescent phenotypes and telomere lengths of peripheral blood T-cells mobilized by acute exercise in humans. Exerc. Immunol. Rev. 2010, 16:40.
70. Sonnenfeld G., Butel J.S., Shearer W.T. Effects of the space flight environment on the immune system. Rev. Environ. Health 2003, 18:1.
71. Stowe R.P., Mehta S.K., Ferrando A.A., Feeback D.L., Pierson D.L. Immune responses and latent herpesvirus reactivation in spaceflight. Aviat. Space Environ. Med. 2001, 72:884.
72. Stowe R.P., Sams C.F., Pierson D.L. Effects of mission duration on neuroimmune responses in astronauts. Aviat. Space Environ. Med. 2003, 74:1281.
73. Stowe R.P., Yetman D.L., Storm W.F., Sams C.F., Pierson D.L. Neuroendocrine and immune responses to 16-day bed rest with realistic launch and landing G profiles. Aviat. Space Environ. Med. 2008, 79:117.
74. Strewe, C., Crucian, B., Mehta, S., Feuerecker, M., Stowe, R., Kaufmann, I., Martignoni, A., Schelling, G., Pierson, D., Chouker, A. Sams, C., 2012. Immune functions during NASA Extreme Environment Mission Operations (NEEMO): the role of hyperoxic stress. In: Life in Space for Life on Earth - 12th European Life Sciences Symposium 33rd Annual International Gravitational Physiology Meeting, vol. June 18-22, Aberdeen, United Kingdom.
75. Stuster J. Bold Endeavours: Lessons from Polar and Space Exploration 2011, Naval Institute Press.
76. Sundaresan A., Risin D., Pellis N.R. Loss of signal transduction and inhibition of lymphocyte locomotion in a ground-based model of microgravity. In Vitro Cell. Dev. Biol. Anim. 2002, 38:118.
77. Taylor G.R., Janney R.P. In vivo testing confirms a blunting of the human cell-mediated immune mechanism during space flight. J. Leukoc. Biol. 1992, 51:129.
78. Uchakin P.N., Cubbage M.L., Sams C.F., Morukov B.V., Larina I.V., Bobrovnik E.B. Effects of the 120 days of head-down bed rest on cytokine secretion and its in vitro modulation by glucocorticoids. J. Gravit. Physiol. 1998, 5:P171.
79. Ward N.E., Pellis N.R., Risin S.A., Risin D. Gene expression alterations in activated human T-cells induced by modeled microgravity. J. Cell. Biochem. 2006, 99:1187.
80. Wise K.C., Manna S.K., Yamauchi K., Ramesh V., Wilson B.L., Thomas R.L., Sarkar S., Kulkarni A.D., Pellis N.R., Ramesh G.T. Activation of nuclear transcription factor-kappaB in mouse brain induced by a simulated microgravity environment. In Vitro Cell. Dev. Biol. Anim. 2005, 41:118.
81. Yamauchi K., Hales N.W., Robinson S.M., Niehoff M.L., Ramesh V., Pellis N.R., Kulkarni A.D. Dietary nucleotides prevent decrease in cellular immunity in ground-based microgravity analog. J. Appl. Physiol. 2002, 93:161.
82. Zhou Y., Ni H., Li M., Sanzari J.K., Diffenderfer E.S., Lin L., Kennedy A.R., Weissman D. Effect of solar particle event radiation and hindlimb suspension on gastrointestinal tract bacterial translocation and immune activation. PLoS One 2012, 7:e44329.
83. Zwart S.R., Mehta S.K., Ploutz-Snyder R., Bourbeau Y., Locke J.P., Pierson D.L., Smith S.M. Response to vitamin D supplementation during Antarctic winter is related to BMI, and supplementation can mitigate Epstein-Barr Virus Reactivation. J. Nutr. 2011, 141:692.