Glucocorticoids and macrophage migration inhibitory factor (MIF) are neuroendocrine modulators of inflammation and neuropathic pain after spinal cord injury

Seminars in Immunology

Volumn 26, Issue 5, 2014, Pages 409-414

  Lerch, Jessica K ^a   Puga, Denise A ^a   Bloom, Ona ^b   Popovich, Phillip G ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

Glucocorticoid; Inflammation; Macrophage migration inhibitory factor (MIF); Neuropathic pain; Spinal cord injury

Indexed keywords

GLUCOCORTICOID; MACROPHAGE MIGRATION INHIBITION FACTOR; GLUCOCORTICOID RECEPTOR; ISOMERASE; MIF PROTEIN, HUMAN;

HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; INFLAMMATION; NERVE CELL PLASTICITY; NEUROENDOCRINOLOGY; NEUROPATHIC PAIN; NONHUMAN; REGULATORY MECHANISM; REVIEW; SPINAL CORD INJURY; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; IMMUNOLOGY; METABOLISM; NEURALGIA; PATHOLOGY; PROTEIN ANALYSIS; SIGNAL TRANSDUCTION;

ANIMALS; GENE EXPRESSION REGULATION; GLUCOCORTICOIDS; HUMANS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; INFLAMMATION; INTRAMOLECULAR OXIDOREDUCTASES; MACROPHAGE MIGRATION-INHIBITORY FACTORS; NEURALGIA; PITUITARY-ADRENAL SYSTEM; PROTEIN INTERACTION MAPPING; RECEPTORS, GLUCOCORTICOID; SIGNAL TRANSDUCTION; SPINAL CORD INJURIES;

EID: 84922693822     PISSN: 10445323     EISSN: 10963618     Source Type: Journal    
DOI: 10.1016/j.smim.2014.03.004     Document Type: Review

References (95)

1. Purves D., Augustine G., Fitzpatrick D., Katz L., LaMantia A.-S., McNamara J., et al. Neuroscience 2001, Sinauer Associates, Sunderland, MA. 2nd ed.
2. Revollo J.R., Cidlowski J.A. Mechanisms generating diversity in glucocorticoid receptor signaling. Ann N Y Acad Sci 2009, 1179:167-178.
3. Popoli M., Yan Z., McEwen B.S., Sanacora G. The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission. Nat Rev Neurosci 2012, 13:22-37.
4. Hall E.D. Antioxidant therapies for acute spinal cord injury. Neurotherapeutics 2011, 8:152-167.
5. Cruse J.M., Keith J.C., Bryant M.L., Lewis R.E. Immune system-neuroendocrine dysregulation in spinal cord injury. Immunol Res 1996, 15:306-314.
6. Lucin K.M., Sanders V.M., Jones T.B., Malarkey W.B., Popovich P.G. Impaired antibody synthesis after spinal cord injury is level dependent and is due to sympathetic nervous system dysregulation. Exp Neurol 2007, 207:75-84.
7. Deroche-Gamonet V., Sillaber I., Aouizerate B., Izawa R., Jaber M., Ghozland S., et al. The glucocorticoid receptor as a potential target to reduce cocaine abuse. J Neurosci Off J Soc Neurosci 2003, 23:4785-4790.
8. Kellendonk C., Gass P., Kretz O., Schutz G., Tronche F. Corticosteroid receptors in the brain: gene targeting studies. Brain Res Bull 2002, 57:73-83.
9. Busillo J.M., Cidlowski J.A. The five Rs of glucocorticoid action during inflammation: ready, reinforce, repress, resolve, and restore. Trends Endocrinol Metab: TEM 2013, 24:109-119.
10. Glezer I., Rivest S. Glucocorticoids: protectors of the brain during innate immune responses. Neurosci Rev J Bring Neurobiol Neurol psychiatry 2004, 10:538-552.
11. Sorrells S.F., Caso J.R., Munhoz C.D., Hu C.K., Tran K.V., Miguel Z.D., et al. Glucocorticoid signaling in myeloid cells worsens acute CNS injury and inflammation. J Neurosci Off J Soc Neurosci 2013, 33:7877-7889.
12. Sorrells S.F., Caso J.R., Munhoz C.D., Sapolsky R.M. The stressed CNS: when glucocorticoids aggravate inflammation. Neuron 2009, 64:33-39.
13. Nesan D., Vijayan M.M. Role of glucocorticoid in developmental programming: evidence from zebrafish. Gen Comp Endocrinol 2013, 181:35-44.
14. Smith L.K., Tandon A., Shah R.R., Mav D., Scoltock A.B., Cidlowski J.A. Deep sequencing identification of novel glucocorticoid-responsive miRNAs in apoptotic primary lymphocytes. PLoS ONE 2013, 8:e78316.
15. Oakley R.H., Revollo J., Cidlowski J.A. Glucocorticoids regulate arrestin gene expression and redirect the signaling profile of G protein-coupled receptors. Proc Natl Acad Sci U S A 2012, 109:17591-17596.
16. Finnerup N.B., Baastrup C. Spinal cord injury pain: mechanisms and management. Curr Pain Headache Rep 2012, 16:207-216.
17. Jensen M.P., Hoffman A.J., Cardenas D.D. Chronic pain in individuals with spinal cord injury: a survey and longitudinal study. Spinal Cord 2005, 43:704-712.
18. Siddall P.J., McClelland J.M., Rutkowski S.B., Cousins M.J. A longitudinal study of the prevalence and characteristics of pain in the first 5 years following spinal cord injury. Pain 2003, 103:249-257.
19. Schonenberg M., Reimitz M., Jusyte A., Maier D., Badke A., Hautzinger M. Depression, posttraumatic stress, and risk factors following spinal cord injury. Int J Behav Med 2014, 21:169-176.
20. Migliorini C., Callaway L., New P. Preliminary investigation into subjective well-being, mental health, resilience, and spinal cord injury. J Spinal Cord Med 2013, 36:660-665.
21. Wang S., Lim G., Zeng Q., Sung B., Ai Y., Guo G., et al. Expression of central glucocorticoid receptors after peripheral nerve injury contributes to neuropathic pain behaviors in rats. J Neurosci Off J Soc Neurosci 2004, 24:8595-8605.
22. Ashkinazi I., Vershinina E.A. Pain sensitivity in chronic psychoemotional stress in humans. Neurosci Behav Physiol 1999, 29:333-337.
23. DeLeo J.A. Basic science of pain. J Bone Joint Surg Am Vol 2006, 88(Suppl. 2):58-62.
24. Greco C.M., Rudy T.E., Manzi S. Effects of a stress-reduction program on psychological function, pain, and physical function of systemic lupus erythematosus patients: a randomized controlled trial. Arthritis Rheum 2004, 51:625-634.
25. Nicholson K., Martelli M.F. The problem of pain. J Head Trauma Rehabil 2004, 19:2-9.
26. Turner J.A., Jensen M.P., Warms C.A., Cardenas D.D. Catastrophizing is associated with pain intensity, psychological distress, and pain-related disability among individuals with chronic pain after spinal cord injury. Pain 2002, 98:127-134.
27. Kingery W.S., Agashe G.S., Sawamura S., Davies M.F., Clark J.D., Maze M. Glucocorticoid inhibition of neuropathic hyperalgesia and spinal Fos expression. Anesth Analg 2001, 92:476-482.
28. Shah A., Kirchner J.S. Complex regional pain syndrome. Foot Ankle Clin 2011, 16:351-366.
29. Takasaki I., Kurihara T., Saegusa H., Zong S., Tanabe T. Effects of glucocorticoid receptor antagonists on allodynia and hyperalgesia in mouse model of neuropathic pain. Eur J Pharmacol 2005, 524:80-83.
30. Chaplan S.R., Malmberg A.B., Yaksh T.L. Efficacy of spinal NMDA receptor antagonism in formalin hyperalgesia and nerve injury evoked allodynia in the rat. J Pharmacol Exp Ther 1997, 280:829-838.
31. Theodosiou M., Rush R.A., Zhou X.F., Hu D., Walker J.S., Tracey D.J. Hyperalgesia due to nerve damage: role of nerve growth factor. Pain 1999, 81:245-255.
32. Sah D.W., Ossipo M.H., Porreca F. Neurotrophic factors as novel therapeutics for neuropathic pain. Nat Rev Drug Discov 2003, 2:460-472.
33. Wang S., Lim G., Zeng Q., Sung B., Yang L., Mao J. Central glucocorticoid receptors modulate the expression and function of spinal NMDA receptors after peripheral nerve injury. J Neurosci 2005, 25:488-495.
34. Wang S., Lim G., Yang L., Sung B., Mao J. Downregulation of spinal glutamate transporter EAAC1 following nerve injury is regulated by central glucocorticoid receptors in rats. Pain 2006, 120:78-85.
35. Wang S., Lim G., Mao J., Sung B., Yang L. Central glucocorticoid receptors regulate the upregulation of spinal cannabinoid-1 receptors after peripheral nerve injury in rats. Pain 2007, 131:96-105.
36. Alexander J.K., DeVries A.C., Kigerl K.A., Dahlman J.M., Popovich P.G. Stress exacerbates neuropathic pain via glucocorticoid and NMDA receptor activation. Brain Behav Immun 2009, 23:851-860.
37. Yan P., Xu J., Li Q., Chen S., Kim G.M., Hsu C.Y., et al. Glucocorticoid receptor expression in the spinal cord after traumatic injury in adult rats. J Neurosci 1999, 19:9355-9363.
38. Zhang Y., Guan Z., Reader B., Shawler T., Mandrekar-Colucci S., Huang K., et al. Autonomic dysreflexia causes chronic immune suppression after spinal cord injury. J Neurosci 2013, 33:12970-12981.
39. Bloom B.R., Bennett B. Mechanism of a reaction in vitro associated with delayed-type hypersensitivity. Science 1966, 153:80-82.
40. Calandra T., Roger T. Macrophage migration inhibitory factor: a regulator of innate immunity. Nat Rev Immunol 2003, 3:791-800.
41. Alexander J.K., Cox G.M., Tian J.B., Zha A.M., Wei P., Kigerl K.A., et al. Macrophage migration inhibitory factor (MIF) is essential for inflammatory and neuropathic pain and enhances pain in response to stress. Exp Neurol 2012, 236:351-362.
42. Honma N., Koseki H., Akasaka T., Nakayama T., Taniguchi M., Serizawa I., et al. Deficiency of the macrophage migration inhibitory factor gene has no significant effect on endotoxaemia. Immunology 2000, 100:84-90.
43. Lue H., Kleemann R., Calandra T., Roger T., Bernhagen J. Macrophage migration inhibitory factor (MIF): mechanisms of action and role in disease. Microb Infect/Institut Pasteur 2002, 4:449-460.
44. Bucala R. Signal transduction. A most interesting factor. Nature 2000, 408:146-147.
45. Kudrin A., Ray D. Cunning factor: macrophage migration inhibitory factor as a redox-regulated target. Immunol Cell Biol 2008, 86:232-238.
46. Baugh J.A., Chitnis S., Donnelly S.C., Monteiro J., Lin X., Plant B.J., et al. A functional promoter polymorphism in the macrophage migration inhibitory factor (MIF) gene associated with disease severity in rheumatoid arthritis. Gen Immun 2002, 3:170-176.
47. Donn R.P., Barrett J.H., Farhan A., Stopford A., Pepper L., Shelley E., et al. Cytokine gene polymorphisms and susceptibility to juvenile idiopathic arthritis. British Paediatric Rheumatology Study Group. Arthritis Rheum 2001, 44:802-810.
48. Shi X., Leng L., Wang T., Wang W., Du X., Li J., et al. CD44 is the signaling component of the macrophage migration inhibitory factor-CD74 receptor complex. Immunity 2006, 25:595-606.
49. Schwartz V., Lue H., Kraemer S., Korbiel J., Krohn R., Ohl K., et al. A functional heteromeric MIF receptor formed by CD74 and CXCR4. FEBS Lett 2009, 583:2749-2757.
50. Mitchell R.A., Metz C.N., Peng T., Bucala R. Sustained mitogen-activated protein kinase (MAPK) and cytoplasmic phospholipase A2 activation by macrophage migration inhibitory factor (MIF). Regulatory role in cell proliferation and glucocorticoid action. J Biol Chem 1999, 274:18100-18106.
51. Leng L., Metz C.N., Fang Y., Xu J., Donnelly S., Baugh J., et al. MIF signal transduction initiated by binding to CD74. J Exp Med 2003, 197:1467-1476.
52. Lue H., Thiele M., Franz J., Dahl E., Speckgens S., Leng L., et al. Macrophage migration inhibitory factor (MIF) promotes cell survival by activation of the Akt pathway and role for CSN5/JAB1 in the control of autocrine MIF activity. Oncogene 2007, 26:5046-5059.
53. Markus A., Zhong J., Snider W.D. Raf and akt mediate distinct aspects of sensory axon growth. Neuron 2002, 35:65-76.
54. Lue H., Kapurniotu A., Fingerle-Rowson G., Roger T., Leng L., Thiele M., et al. Rapid and transient activation of the ERK MAPK signalling pathway by macrophage migration inhibitory factor (MIF) and dependence on JAB1/CSN5 and Src kinase activity. Cell Signal 2006, 18:688-703.
55. Samuels I.S., Karlo J.C., Faruzzi A.N., Pickering K., Herrup K., Sweatt J.D., et al. Deletion of ERK2 mitogen-activated protein kinase identifies its key roles in cortical neurogenesis and cognitive function. J Neurosci 2008, 28:6983-6995.
56. Obata K., Yamanaka H., Dai Y., Tachibana T., Fukuoka T., Tokunaga A., et al. Differential activation of extracellular signal-regulated protein kinase in primary afferent neurons regulates brain-derived neurotrophic factor expression after peripheral inflammation and nerve injury. J Neurosci 2003, 23:4117-4126.
57. Obata K., Yamanaka H., Kobayashi K., Dai Y., Mizushima T., Katsura H., et al. Role of mitogen-activated protein kinase activation in injured and intact primary afferent neurons for mechanical and heat hypersensitivity after spinal nerve ligation. J Neurosci 2004, 24:10211-10222.
58. Kleemann R., Hausser A., Geiger G., Mischke R., Burger-Kentischer A., Flieger O., et al. Intracellular action of the cytokine MIF to modulate AP-1 activity and the cell cycle through Jab1. Nature 2000, 408:211-216.
59. Ji R.R., Baba H., Brenner G.J., Woolf C.J. Nociceptive-specific activation of ERK in spinal neurons contributes to pain hypersensitivity. Nat Neurosci 1999, 2:1114-1119.
60. Stein A., Panjwani A., Sison C., Rosen L., Chugh R., Metz C., et al. Pilot study: elevated circulating levels of the proinflammatory cytokine macrophage migration inhibitory factor in patients with chronic spinal cord injury. Arch Phys Med Rehabil 2013, 94:1498-1507.
61. Popp J., Bacher M., Kolsch H., Noelker C., Deuster O., Dodel R., et al. Macrophage migration inhibitory factor in mild cognitive impairment and Alzheimer's disease. J Psychiatr Res 2009, 43:749-753.
62. Craig-Schapiro R., Kuhn M., Xiong C., Pickering E.H., Liu J., Misko T.P., et al. Multiplexed immunoassay panel identifies novel CSF biomarkers for Alzheimer's disease diagnosis and prognosis. PLoS ONE 2011, 6:e18850.
63. Nicoletti A., Fagone P., Donzuso G., Mangano K., Dibilio V., Caponnetto S., et al. Parkinson's disease is associated with increased serum levels of macrophage migration inhibitory factor. Cytokine 2011, 55:165-167.
64. Denkinger C.M., Denkinger M., Kort J.J., Metz C., Forsthuber T.G. In vivo blockade of macrophage migration inhibitory factor ameliorates acute experimental autoimmune encephalomyelitis by impairing the homing of encephalitogenic T cells to the central nervous system. J Immunol 2003, 170:1274-1282.
65. Hagman S., Raunio M., Rossi M., Dastidar P., Elovaara I. Disease-associated inflammatory biomarker profiles in blood in different subtypes of multiple sclerosis: prospective clinical and MRI follow-up study. J Neuroimmunol 2011, 234:141-147.
66. Bernhagen J., Calandra T., Mitchell R.A., Martin S.B., Tracey K.J., Voelter W., et al. MIF is a pituitary-derived cytokine that potentiates lethal endotoxaemia. Nature 1993, 365:756-759.
67. Leech M., Metz C., Santos L., Peng T., Holdsworth S.R., Bucala R., et al. Involvement of macrophage migration inhibitory factor in the evolution of rat adjuvant arthritis. Arthritis Rheum 1998, 41:910-917.
68. Mikulowska A., Metz C.N., Bucala R., Holmdahl R. Macrophage migration inhibitory factor is involved in the pathogenesis of collagen type II-induced arthritis in mice. J Immunol 1997, 158:5514-5517.
69. Lan H.Y., Yang N., Nikolic-Paterson D.J., Yu X.Q., Mu W., Isbel N.M., et al. Expression of macrophage migration inhibitory factor in human glomerulonephritis. Kidney Int 2000, 57:499-509.
70. Brown F.G., Nikolic-Paterson D.J., Hill P.A., Isbel N.M., Dowling J., Metz C.M., et al. Urine macrophage migration inhibitory factor reflects the severity of renal injury in human glomerulonephritis. J Am Soc Nephrol 2002, 13(Suppl. 1):S7-S13.
71. Schober A., Bernhagen J., Thiele M., Zeiffer U., Knarren S., Roller M., et al. Stabilization of atherosclerotic plaques by blockade of macrophage migration inhibitory factor after vascular injury in apolipoprotein E-deficient mice. Circulation 2004, 109:380-385.
72. Burger-Kentischer A., Goebel H., Seiler R., Fraedrich G., Schaefer H.E., Dimmeler S., et al. Expression of macrophage migration inhibitory factor in different stages of human atherosclerosis. Circulation 2002, 105:1561-1566.
73. Cvetkovic I., Al-Abed Y., Miljkovic D., Maksimovic-Ivanic D., Roth J., Bacher M., et al. Critical role of macrophage migration inhibitory factor activity in experimental autoimmune diabetes. Endocrinology 2005, 146:2942-2951.
74. Stosic-Grujicic S., Stojanovic I., Maksimovic-Ivanic D., Momcilovic M., Popadic D., Harhaji L., et al. Macrophage migration inhibitory factor (MIF) is necessary for progression of autoimmune diabetes mellitus. J Cell Physiol 2008, 215:665-675.
75. Makino A., Nakamura T., Hirano M., Kitta Y., Sano K., Kobayashi T., et al. High plasma levels of macrophage migration inhibitory factor are associated with adverse long-term outcome in patients with stable coronary artery disease and impaired glucose tolerance or type 2 diabetes mellitus. Atherosclerosis 2010, 213:573-578.
76. Koda M., Nishio Y., Hashimoto M., Kamada T., Koshizuka S., Yoshinaga K., et al. Up-regulation of macrophage migration-inhibitory factor expression after compression-induced spinal cord injury in rats. Acta Neuropathol 2004, 108:31-36.
77. Nishio Y., Koda M., Hashimoto M., Kamada T., Koshizuka S., Yoshinaga K., et al. Deletion of macrophage migration inhibitory factor attenuates neuronal death and promotes functional recovery after compression-induced spinal cord injury in mice. Acta Neuropathol 2009, 117:321-328.
78. Chalimoniuk M., King-Pospisil K., Metz C.N., Toborek M. Macrophage migration inhibitory factor induces cell death and decreases neuronal nitric oxide expression in spinal cord neurons. Neuroscience 2006, 139:1117-1128.
79. Bacher M., Meinhardt A., Lan H.Y., Dhabhar F.S., Mu W., Metz C.N., et al. MIF expression in the rat brain: implications for neuronal function. Mol Med 1998, 4:217-230.
80. Marchand F., Perretti M., McMahon S.B. Role of the immune system in chronic pain. Nat Rev Neurosci 2005, 6:521-532.
81. Scholz J., Woolf C.J. The neuropathic pain triad: neurons, immune cells and glia. Nat Neurosci 2007, 10:1361-1368.
82. Wang F., Wu H., Xu S., Guo X., Yang J., Shen X. Macrophage migration inhibitory factor activates cyclooxygenase 2-prostaglandin E2 in cultured spinal microglia. Neurosci Res 2011, 71:210-218.
83. Walters E.T. Nociceptors as chronic drivers of pain and hyperreflexia after spinal cord injury: an adaptive-maladaptive hyperfunctional state hypothesis. Front Integr Physiol 2012, 3:1-13.
84. Bank L.M., Bianchi L.M., Ebisu F., Lerman-Sinkoff D., Smiley E.C., Shen Y.C., et al. Macrophage migration inhibitory factor acts as a neurotrophin in the developing inner ear. Development 2012, 139:4666-4674.
85. Nishio Y., Nishihira J., Ishibashi T., Kato H., Minami A. Role of macrophage migration inhibitory factor (MIF) in peripheral nerve regeneration: anti-MIF antibody induces delay of nerve regeneration and the apoptosis of Schwann cells. Mol Med 2002, 8:509-520.
86. Padovani-Claudio D.A., Liu L., Ransohoff R.M., Miller R.H. Alterations in the oligodendrocyte lineage, myelin, and white matter in adult mice lacking the chemokine receptor CXCR2. Glia 2006, 54:471-483.
87. Nishino T., Bernhagen J., Shiiki H., Calandra T., Dohi K., Bucala R. Localization of macrophage migration inhibitory factor (MIF) to secretory granules within the corticotrophic and thyrotrophic cells of the pituitary gland. Mol Med 1995, 1:781-788.
88. Calandra T., Bernhagen J., Metz C.N., Spiegel L.A., Bacher M., Donnelly T., et al. MIF as a glucocorticoid-induced modulator of cytokine production. Nature 1995, 377:68-71.
89. Bruhn A., Verdant C., Vercruysse V., Su F., Vray B., Vincent J.L. Effects of dexamethasone on macrophage migration inhibitory factor production in sepsis. Shock 2006, 26:169-173.
90. Nikolic I., Vujicic M., Saksida T., Berki T., Stosic-Grujicic S., Stojanovic I. The role of endogenous glucocorticoids in glucose metabolism and immune status of MIF-deficient mice. Eur J Pharmacol 2013, 714:498-506.
91. Waeber G., Thomopson N., Chautard T., Steinmann P., Nicod P., Pralong F.P., et al. Transcriptional activation of the macrophage migration inhibitory factor gene by corticotropin-releasing factor is mediated by the cyclic adensosine 3',5'-mono-phosphate responsive element-binding protein CREB in pituitary cells. Mol Endocrinol 1998, 12:689-705.
92. Bacher M., Weihe E., Dietzschold B., Meinhardt A., Vedder H., Gemsa D., et al. Borna disease virus-induced accumulation of macrophage migration inhibitory factor in rat brain astrocytes is associated with inhibition of macrophage infiltration. Glia 2002, 37:291-306.
93. Yang N., Nikolic-Paterson D.J., Ng Y.Y., Mu W., Metz C., Bacher M., et al. Reversal of established rat crescentic glomerulonephritis by blockade of macrophage migration inhibitory factor (MIF): potential role of MIF in regulating glucocorticoid production. Mol Med 1998, 4:413-424.
94. Miyauchi T., Tsuruta R., Fujita M., Kaneko T., Kasaoka S., Maekawa T. Serum macrophage migration inhibitory factor reflects adrenal function in the hypothalamo-pituitary-adrenal axis of septic patients: an observational study. BMC Infect Dis 2009, 9:209.
95. Pastrana E.A., Saavedra F.M., Murray G., Estronza S., Rolston J.D., Rodriguez-Vega G. Acute adrenal insufficiency in cervical spinal cord injury. World Neurosurg 2012, 77:561-563.