Stress-induced facilitation of host response to bacterial challenge in F344 rats is dependent on extracellular heat shock protein 72 and independent of alpha beta T cells

Stress

Volumn 15, Issue 6, 2012, Pages 637-646

  Campisi, Jay ^a   Sharkey, Craig ^b   Johnson, John D ^c   Asea, Alexzander ^d   Maslanik, Thomas ^b   Bernstein Hanley, Isaac ^b   Fleshner, Monika ^b  

^a REGIS UNIVERSITY   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c KENT STATE UNIVERSITY   (United States)

^d TEXAS A M COLLEGE OF MEDICINE   (United States)

Author keywords

Athymic nude rat; E. coli; Hsp72; Immunomodulation; Inflammation; Innate immunity

Indexed keywords

HEAT SHOCK PROTEIN 72;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD LEVEL; CONTROLLED STUDY; ELECTRIC SHOCK; ESCHERICHIA COLI; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOMODULATION; INFLAMMATION; INNATE IMMUNITY; MALE; NONHUMAN; NUDE RAT; PRIORITY JOURNAL; RAT; STRESS; T LYMPHOCYTE;

ANIMALS; ELECTROSHOCK; ESCHERICHIA COLI INFECTIONS; HSP72 HEAT-SHOCK PROTEINS; INFLAMMATION; MALE; RATS; RATS, INBRED F344; RATS, NUDE; STRESS, PSYCHOLOGICAL; T-LYMPHOCYTES;

EID: 84867363351     PISSN: 10253890     EISSN: 16078888     Source Type: Journal    
DOI: 10.3109/10253890.2011.653596     Document Type: Article

References (93)

1. Ader R. 2007. Psychoneuroimmunology. Elsevier Academic Press.
2. Asea A. 2003. Chaperokine-induced signal transduction pathways. Exerc Immunol Rev 9:25-33.
3. Asea A, Kabingu E, Stevenson MA, Calderwood SK. 2000. HSP70 peptide-bearing and peptide-negative preparations act as chaperokines. Cell Stress Chaperones 5:425-431. (Pubitemid 32057493)
4. Bailey MT, Dowd SE, Galley JD, Hufnagle AR, Allen RG, Lyte M. 2011. Exposure to a social stressor alters the structure of the intestinal microbiota: Implications for stressor-induced immu-nomodulation. Brain Behav Immun 25:397-407.
5. Bailey MT, Engler H, Sheridan JF. 2006. Stress induces the translocation of cutaneous and gastrointestinal microflora to secondary lymphoid organs of C57BL/6 mice. J Neuroimmunol 171:29-37. (Pubitemid 41832275)
6. Bethke K, Staib F, Distler M, Schmitt U, Jonuleit H, Enk AH, Galle PR, Heike M. 2002. Different efficiency of heat shock proteins (HSP) to activate human monocytes and dendritic cells: Superiority of HSP60. J Immunol 169:6141-6148. (Pubitemid 36903458)
7. Breloer M, Dorner B, More SH, Roderian T, Fleischer B, von Bonin A. 2001. Heat shock proteins as "danger signals": Eukaryotic Hsp60 enhances and accelerates antigen-specific IFN-gamma production in T cells. Eur J Immunol 31:2051-2059. (Pubitemid 32640721)
8. Brown DA, Johnson MS, Armstrong CJ, Lynch JM, Caruso NM, Ehlers LB, Fleshner M, Spencer RL, Moore RL. 2007. Short-term treadmill running in the rat: What kind of stressor is it? J Appl Physiol 103:1979-1985. (Pubitemid 350232380)
9. Bugajska J, Widerszal-Bazyl M, Radkiewicz P, Pasierski T, Szulczyk GA, Zabek J, Wojciechowska B, Jedryka-Goral A. 2008. Perceived work-related stress and early atherosclerotic changes in healthy employees. Int Arch Occup Environ Health 81: 1037-1043.
10. Calderwood SK, Gong J, Theriault JR, Mambula SS, Gray PJ, Jr. 2008. Cell stress proteins: Novel immunotherapeutics. Novartis Found Symp 291:115-131, discussion 131-140.
11. Campisi J, Fleshner M. 2003. The role of extracellular Hsp72 in acute stress-induced potentiation of innate immunity in physically active rats. J Appl Physiol 94:43-52. (Pubitemid 36014294)
12. Campisi J, Hansen MK, O'Connor KA, Biedenkapp JC, Watkins LR, Maier SF, Fleshner M. 2003a. Circulating cytokines and endotoxin are not necessary for the activation of the sickness or corticosterone response produced by peripheral E. coli challenge. J Appl Physiol 95:1873-1882. (Pubitemid 37310370)
13. Campisi J, Leem TH, Fleshner M. 2002. Acute stress decreases inflammation at the site of infection. A role for nitric oxide. Physiol Behav 77:291-299. (Pubitemid 35373884)
14. Campisi J, Leem TH, Fleshner M. 2003b. Stress-induced extracellular Hsp72 is a functionally significant danger signal to the immune system. Cell Stress Chaperones 8:272-286. (Pubitemid 37484722)
15. Campisi J, Leem TH, Greenwood BN, Hansen MK, Moraska A, Higgins K, Smith TP, Fleshner M. 2003c. Habitual physical activity facilitates stress-induced HSP72 induction in brain, peripheral and immune tissues. Am J Physiol 284:520-530.
16. Chen HW, Chou FP, Lue SI, Hsu HK, Yang RC. 1999. Evidence of multi-step regulation of HSP72 expression in experimental sepsis. Shock 12:63-68.
17. Colaco CA. 1998. Towards a unified theory ofimmunity: Dendritic cells, stress proteins and antigen capture. Cell Mol Biol 44: 883-890.
18. Colagiovanni DB, Suniga MA, Frazier JL, Edwards CK, 3rd, Fleshner M, Mc Cay JA, White KL, Jr, Shopp GM. 2000. TNF-alpha blockade by a dimeric TNF type I receptor molecule selectively inhibits adaptive immune responses. Immunophar-macol Immunotoxicol 22:627-651.
19. Davies EL, Bacelar MM, Marshall MJ, Johnson E, Wardle TD, Andrew SM, Williams JH. 2006. Heat shock proteins form part of a danger signal cascade in response to lipopolysaccharide and Gro EL. Clin Exp Immunol 145:183-189. (Pubitemid 43893948)
20. Deak T, Meriwether JL, Fleshner M, Spencer RL, Abouhamze A, Moldawer LL, Grahn RE, Watkins LR, Maier SF. 1997. Evidence that briefstress may induce the acute phase response in rats. Am J Physiol 273:R1998-R2004.
21. Deak T, Nguyen KT, Fleshner M, Watkins LR, Maier SF. 1999. Acute stress may facilitate recovery from a subcutaneous bacterial challenge. Neuroimmunomodulation 6:344-354. (Pubitemid 29418463)
22. Deitch EA, Berg R. 1987. Bacterial translocation from the gut: A mechanism ofinfection. J Burn Care Rehabil 8:475-482. (Pubitemid 18019994)
23. Dhabhar FS, Mc Ewen BS. 1996. Stress-induced enhancement of antigen-specific cell-mediated immunity. J Immunol 156: 2608-2615. (Pubitemid 26091591)
24. El Mezayen R, El Gazzar M, Seeds MC, Mc Call CE, Dreskin SC, Nicolls MR. 2007. Endogenous signals released from necrotic cells augment inflammatory responses to bacterial endotoxin. Immunol Lett 111:36-44. (Pubitemid 47017473)
25. Febbraio MA, Koukoulas I. 2000. HSP72 gene expression progressively increases in human skeletal muscle during prolonged, exhaustive exercise. J Appl Physiol 89:1055-1060. (Pubitemid 32125405)
26. Febbraio MA, Ott P, Nielsen HB, Steensberg A, Keller C, Krustrup P, Secher NH, Pedersen BK. 2002. Exercise induces hepatos-planchnic release of heat shock protein 72 in humans. J Physiol 544:957-962. (Pubitemid 35355972)
27. Fehrenbach E, Passek F, Niess AM, Pohla H, Weinstock C, Dickhuth HH, Northoff H. 2000. HSP expression in human leukocytes is modulated by endurance exercise. Med Sci Sports Exerc 32:592-600. (Pubitemid 30158330)
28. Fleshner M, Campisi J, Amiri L, Diamond DM. 2004. Cat exposure induces both intra- and extra-cellular HSP72: The role of adrenal hormones. Psychoneuroendocrinology 29: 1142-1152. (Pubitemid 38829176)
29. Fleshner M, Campisi J, Deak T, Greenwood BN, Kintzel JA, Leem TH, Smith TP, Sorensen B. 2002. Acute stressor exposure facilitates innate immunity more in physically active than in sedentary rats. Am J Physiol Regul Integr Comp Physiol 282: R1680-R1686. (Pubitemid 34664493)
30. Fleshner M, Campisi J, Johnson JD. 2003. Can exercise stress facilitate innate immunity? A functional role for stress-induced extracellular Hsp72. Exerc Immunol Rev 9:6-24.
31. Fleshner M, Deak T, Nguyen KT, Watkins LR, Maier SF. 2001. Endogenous glucocorticoids play a positive regulatory role in the anti-keyhole limpet hemocyanin in vivo antibody response. JImmunol 166:3813-3819. (Pubitemid 32224906)
32. Fleshner M, Hermann J, Lockwood LL, Watkins LR, Laudenslager ML, Maier SF. 1995. Stressed rats fail to expand the CD45RC + CD4 + (Th1-like) T cell subset in response to KLH: Possible involvement of IFN-gamma. Brain Behav Immun 9:101-112.
33. Fleshner M, Johnson JD, Friedman J. 2007. Extracellular Hsp72: A double-edged sword for host defense. New York, NY: Springer.
34. Fleshner M, Nguyen KT, Cotter CS, Watkins LR, Maier SF. 1998. Acute stressor exposure both suppresses acquired immunity and potentiates innate immunity. Am J Physiol 275: R870-R878.
35. Fleshner M, Sharkey C, Nickerson M, Johnson AD. 2006a. Endogenous extracellular Hsp72 release is an adaptive feature of the acute stress response. In: Ader R, Felton DL, Cohen N, editors. Psychoneuroimmunology. San Diego, CA: Academic Press.
36. Fleshner M, Sharkey CM, Nickerson M, Johnson JD. 2006b. Endogenous extracellular Hsp72 release is an adaptive feature of the acute stress response. In: Ader R, Felton DL, Cohen N, editors. Psychoneuroimmunology. San Diego, CA: Academic Press.
37. Habich C, Baumgart K, Kolb H, Burkart V. 2002. The receptor for heat shock protein 60 on macrophages is saturable, specific, and distinct from receptors for other heat shock proteins. J Immunol 168:569-576. (Pubitemid 34049555)
38. Hartl FU. 1996. Molecular chaperones in cellular protein folding. Nature 381:571-579.
39. Hickman-Miller HD, Hildebrand WH. 2004. The immune response under stress: the role of HSP-derived peptides. Trends Immunol 25:427-433. (Pubitemid 38951084)
40. Horton JW. 1994. Bacterial translocation after burn injury: The contribution of ischemia and permeability changes. Shock 1: 286-290.
41. Johnson JD, Campisi J, Sharkey CM, Kennedy SL, Nickerson M, Fleshner M. 2005. Adrenergic receptors mediate stress-induced elevations in extracellular Hsp72. J Appl Physiol 99:1789-1795. (Pubitemid 41547176)
42. Johnson JD, Fleshner M. 2006. Releasing signals, secretory pathways, and immune function of endogenous extracellular heat shock protein 72. J Leukoc Biol 79:425-434. (Pubitemid 44831219)
43. Katafuchi T, Takaki A, Take S, Kondo T, Yoshimura M. 2003. Endotoxin inhibitor blocks heat exposure-induced expression of brain cytokine m RNA in aged rats. Brain Res Mol Brain Res 118:24-32. (Pubitemid 37238984)
44. Kaufmann SH. 1990. Heat shock proteins and the immune response. Immunol Today 11:129-136. (Pubitemid 20095097)
45. Kennedy SL, Nickerson M, Campisi J, Johnson JD, Smith TP, Sharkey C, Fleshner M. 2005. Splenic norepinephrine depletion following acute stress suppresses in vivo antibody response. JNeuroimmunol 165:150-160. (Pubitemid 40984632)
46. Kiang JG,Tsokos GC. 1998. Heatshockprotein70k Da: Molecular biology, biochemistry, and physiology. Pharmacol Ther 80: 183-201. (Pubitemid 28498227)
47. Kohl J. 2006. Self, non-self, and danger: A complementary view. Adv Exp Med Biol 586:71-94.
48. Kolls JK, Mc Cray PB, Jr, Chan YR. 2008. Cytokine-mediated regulation of antimicrobial proteins. Nat Rev Immunol 8: 829-835.
49. Kregel KC. 2002. Invited Review: Heat shock proteins: Modifying factors in physiological stress responses and acquired thermo- tolerance. J Appl Physiol 92:2177-2186. (Pubitemid 34666449)
50. Lehner T Bergmeier LA, Wang Y, Tao L, Sing M, Spallek R, van der Zee R. 2000. Heat shock proteins generate beta-chemokines which function as innate adjuvants enhancing adaptive immunity. Eur J Immunol 30:594-603. (Pubitemid 30098853)
51. Lehner T Wang Y, Whittall T, Mc Gowan E, Kelly CG, Singh M. 2004. Functional domains of HSP70 stimulate generation of cytokines and chemokines, maturation of dendritic cells and adjuvanticity. Biochem Soc Trans 32:629-632. (Pubitemid 39120401)
52. Manjili MH, Park JE, Facciponte JG, Wang XY, Subjeck Jr. 2006. Immunoadjuvant chaperone, GRP170, induces 'danger signals' upon interaction with dendritic cells. Immunol Cell Biol 84: 203-208. (Pubitemid 43344674)
53. Matzinger P. 1994. Tolerance, danger, and the extended family. Annu Rev Immunol 12:991-1045. (Pubitemid 24140436)
54. Matzinger P. 1998. An innate sense ofdanger. Semin Immunol 10: 399-415. (Pubitemid 28499554)
55. Moraska A, Fleshner M. 2001. Voluntary physical activity prevents stress-induced behavioral depression and anti-KLH antibody suppression. Am J Physiol Regul Integr Comp Physiol 281: R484-R489.
56. Morimoto RI. 1994. The biology of heat shock proteins and molecular chaperones. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
57. Multhoff G. 1997. Heatshockprotein 72 (HSP72), ahyperthermia- inducible immunogenic determinant on leukemic K562 and Ewing's sarcoma cells. Int J Hyperthermia 13:39-48. (Pubitemid 27064999)
58. Multhoff G. 2002. Activation of natural killer cells by heat shock protein 70. Int J Hyperthermia 18:576-585. (Pubitemid 35469189)
59. Multhoff G, Botzler C. 1998. Heat-shock proteins and the immune response. Ann NYAcad Sci 851:86-93. (Pubitemid 28370367)
60. Multhoff G, Botzler C, Wiesnet M, Muller E, Meier T, Wilmanns W, Issels RD. 1995. A stress-inducible 72-k Da heat-shock protein (HSP72) is expressed on the surface of human tumor cells, but not on normal cells. Int J Cancer 61:272-279.
61. Nazli A, Yang PC, Jury J, Howe K, Watson JL, Soderholm JD, Sherman PM, Perdue MH, Mc Kay DM. 2004. Epithelia under metabolic stress perceive commensal bacteria as a threat. Am J Pathol 164:947-957. (Pubitemid 38235476)
62. Nettelbladt CG, Katouli M, Bark T, Svenberg T, Mollby R, Ljungqvist O. 2003. Orally inoculated Escherichia coli strains colonize the gut and increase bacterial translocation after stress in rats. Shock 20:251-256.
63. Nguyen KT, Deak T, Will MJ, Hansen MK, Hunsaker BN, Fleshner M, Watkins LR, Maier SF. 2000. Timecourse and corticosterone sensitivity of the brain, pituitary, and serum interleukin-1beta protein response to acute stress. Brain Res 859:193-201. (Pubitemid 30136088)
64. Nickerson M, Kennedy SL, Johnson JD, Fleshner M. 2006. Sexual dimorphism of the intracellular heat shock protein 72 response. J Appl Physiol 101:566-575. (Pubitemid 44162367)
65. Niess AM, Fehrenbach E, Schlotz E, Sommer M, Angres C, Tschositsch K, Battenfeld N, Golly IC, Biesalski HK, Northoff H, Dickhuth HH. 2002. Effects of RRR-alpha-tocopherol on leukocyte expression of HSP72 in response to exhaustive treadmill exercise. Int J Sports Med 23:445-452. (Pubitemid 35007084)
66. Noessner E, Gastpar R, Milani V, Brandl A, Hutzler PJ, Kuppner MC, Roos M, Kremmer E, Asea A, Calderwood SK, Issels RD. 2002. Tumor-derived heat shock protein 70 peptide complexes are cross-presented by human dendritic cells. J Immunol 169: 5424-5432. (Pubitemid 35291639)
67. Ohashi K, Burkart V, Flohe S, Kolb H. 2000. Cutting edge: Heat shock protein 60 is a putative endogenous ligand of the toll-like receptor-4 complex. J Immunol 164:558-561. (Pubitemid 30043672)
68. Pittet JF, Lee H, Morabito D, Howard MB, Welch WJ, Mackersie RC. 2002. Serum levels of Hsp 72 measured early after trauma correlate with survival. J Trauma 52:611 -617, discussion 617. (Pubitemid 34437214)
69. Pockley AG, Multhoff G 2008. Cell stress proteins in extracellular fluids: Friend or foe? Novartis Found Symp 291:86-95, discussion 96-100, 137-140.
70. Prohaszka Z, Fust G. 2004. Immunological aspects of heat-shock proteins - the optimum stress oflife. Mol Immunol 41:29-44. (Pubitemid 38609394)
71. Prohaszka Z, Singh M, Nagy K, Kiss E, Lakos G, Duba J, Fust G. 2002. Heat shock protein 70 is a potent activator of the human complement system. Cell Stress Chaperones 7:17-22. (Pubitemid 36138900)
72. Quintana FJ, Cohen IR. 2005. Heat shock proteins as endogenous adjuvants in sterile and septic inflammation. J Immunol 175: 2777-2782. (Pubitemid 41170492)
73. Rojas IG, Padgett DA, Sheridan JF, Marucha PT. 2002. Stress-induced susceptibility to bacterial infection during cutaneous wound healing. Brain Behav Immun 16:74-84. (Pubitemid 35435455)
74. Rolstad B. 2001. The athymic nude rat: An animal experimental model to reveal novel aspects of innate immune responses? Immunol Rev 184:136-144. (Pubitemid 34123771)
75. Shi Y, Galusha SA, Rock KL. 2006. Cutting edge: Elimination of an endogenous adjuvant reduces the activation of CD8 T lymphocytes to transplanted cells and in an autoimmune diabetes model. J Immunol 176:3905-3908. (Pubitemid 44264366)
76. Srivastava P. 2002. Roles of heat-shock proteins in innate and adaptive immunity. Nat Rev Immunol 2:185-194. (Pubitemid 37328765)
77. Srivastava PK, Udono H, Blachere NE, Li Z. 1994. Heat shock proteins transfer peptides during antigen processing and CTL priming. Immunogenetics 39:93-98. (Pubitemid 23344809)
78. Svensson PA, Asea A, Englund MC, Bausero MA, Jernas M, Wiklund O, Ohlsson BG, Carlsson LM, Carlsson B. 2006. Major role of HSP70 as a paracrine inducer of cytokine production in human oxidized LDL treated macrophages. Atherosclerosis 185:32-38. (Pubitemid 43117548)
79. Todryk SM, Melcher AA, Dalgleish AG, Vile RG. 2000. Heat shock proteins refine the danger theory. Immunology 99:334-337. (Pubitemid 30137696)
80. Udelsman R, Blake MJ, Stagg CA, Li DG, Putney DJ, Holbrook NJ. 1993. Vascular heat shock protein expression in response to stress. Endocrine and autonomic regulation of this age-dependent response. J Clin Invest 91:465-473. (Pubitemid 23064130)
81. Udelsman R, Blake MJ, Holbrook NJ. 1991. Molecular response to surgical stress: Specific and simultaneous heat shock protein induction in the adrenal cortex, aorta, and vena cava. Surgery 110:1125-1131.
82. Vabulas RM, Ahmad-Nejad P, Ghose S, Kirschning CJ, Issels RD, Wagner H. 2002. HSP70 as endogenous stimulus of the Toll/ interleukin-1 receptor signal pathway. J Biol Chem 277: 15107-15112. (Pubitemid 34952589)
83. Van Eden W, Koets A, van Kooten P, Prakken B, van der Zee R. 2003. Immunopotentiating heat shock proteins: Negotiators between innate danger and control of autoimmunity. Vaccine 21: 897-901. (Pubitemid 36126424)
84. Van Eden W, van der Zee R, Prakken B. 2005. Heat-shock proteins induce T-cell regulation of chronic inflammation. Nat Rev Immunol 5:318-330. (Pubitemid 40516157)
85. Velin AK, Ericson AC, Braaf Y, Wallon C, Soderholm JD. 2004. Increased antigen and bacterial uptake in follicle associated epithelium induced by chronic psychological stress in rats. Gut 53:494-500. (Pubitemid 38372972)
86. Walsh RC, Koukoulas I, Garnham A, Moseley PL, Hargreaves M, Febbraio MA. 2001. Exercise increases serum Hsp72 in humans. Cell Stress Chaperones 6:386-393. (Pubitemid 33123492)
87. Wang Y, Seidl T, Whittall T, Babaahmady K, Lehner T. 2010. Stress-activated dendritic cells interact with CD4 + T cells to elicit homeostatic memory. Eur J Immunol 40: 1628-1638.
88. Wells AD, Rai SK, Salvato MS, Band H, Malkovsky M. 1998. Hsp72-mediated augmentation of MHC class I surface expression and endogenous antigen presentation. Int Immunol 10:609-617. (Pubitemid 28221462)
89. Whitham M, Fortes MB. 2008. Heat shock protein 72: Release and biological significance during exercise. Front Biosci 13: 1328-1339. (Pubitemid 351594713)
90. Yokota S, Fujii N. 2010. Immunomodulatory activity ofextracellu- lar heat shock proteins and their autoantibodies. Microbiol Immunol 54:299-307.
91. Yoo CG, Lee S, Lee CT, Kim YW, Han SK, Shim YS. 2000. Anti- inflammatory effect of heat shock protein induction is related to stabilization of I kappa B alpha through preventing I kappa B kinase activation in respiratory epithelial cells. J Immunol 164: 5416-5423. (Pubitemid 30305224)
92. Zampell JC, Yan A, Avraham T, Andrade V, Malliaris S, Aschen S, Rockson SG, Mehrara BJ. 2011. Temporal and spatial patterns of endogenous danger signal expression after wound healing and in response to lymphedema. Am J Physiol Cell Physiol 300: C1107-C1121.
93. Zedler S, Faist E. 2006. The impact of endogenous triggers on trauma-associated inflammation. Curr Opin Crit Care 12: 595-601. (Pubitemid 44673437)