Time-and dose-dependent neuroprotective effects of sex steroid hormones on inflammatory cytokines after a traumatic brain injury

Journal of Neurotrauma

Volumn 30, Issue 1, 2013, Pages 47-54

  Sarkaki, Ali Reza ^a   Haddad, Mohammad Khaksari ^b   Soltani, Zahra ^c   Shahrokhi, Nader ^b   Mahmoodi, Mehdi ^d  

^a AHVAZ JUNDISHAPUR UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b KERMAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c KERMAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^d RAFSANJAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

IL 1 ; IL 6; TGF ; TNF ; traumatic brain injury

Indexed keywords

ESTRADIOL; INTERLEUKIN 1BETA; INTERLEUKIN 6; PROGESTERONE; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BRAIN PROTECTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOSE TIME EFFECT RELATION; DRUG EFFECT; DRUG MEGADOSE; FEMALE; LOW DRUG DOSE; NONHUMAN; RAT; SINGLE DRUG DOSE; TRAUMATIC BRAIN INJURY;

ANIMALS; BRAIN INJURIES; CYTOKINES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTROGENS; FEMALE; INFLAMMATION MEDIATORS; NEUROPROTECTIVE AGENTS; PROGESTERONE; RATS; TIME FACTORS;

EID: 84871479690     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2010.1686     Document Type: Article

References (58)

1. Ahmadmolaie, L., Khaksari, M., Sepehri, G., Dabiri, S., Asadikaram, G., Mahmodi, M., and Shahrokhi, N. (2007). Comparison of the effects of progesterone, allopregnanolone and gender on supressing edema formation after traumatic brain injury. J. kerman university of Medical sciences 15, 47-59.
2. Bartfai, T., Sanchez-Alavez, M., Andell-Jonsson, S., Schultzberg, M., Vezzani, A., Danielsson, E., and Conti, B. (2007). Interleukin-1 system in CNS stress: seizures, fever and neurotrauma. Ann. N. Y. Acad. Sci. 1113, 173-17.
3. Chen, G., Shi, J., Jin, W., Wang, L., Xie, W., Sun, J., and Hang, C. (2008). Progesterone administration modulates TLRs/NF-kappaB signaling pathway in rat brain after cortical contusion. Ann. Clin. Lab. Sci. 38, 65-74.
4. Chiaretti, A., Antonelli, A., Riccardi, R., Genovese, O., Pezzotti, P., Di Rocco, C., Tortorolo, L., and Piedimonte, G. (2008). Nerve growth factor expression correlates with severity and outcome of traumatic brain injury in children. Eur. J. Paediatr. Neurol. 12, 195-204.
5. Crandall, C., Palla, S., Reboussin, B., Hu, P., Barrett-Connor, E., Reuben, D., and Greendale, G. (2006). Cross-sectional association between markers of inflammation and serum sex steroid levels in the postmen-opausal estrogen/progestin interventions trial. J. Womens Health 15, 14-23.
6. Cutler, S. M., Cekic, M., Miller, D. M., Wali, B., VanLandingham, J. W., and Stein, D. G. (2007). Progesterone improves acute recovery after traumatic brain injury in the aged rat. J. Neurotrauma 24, 1475-1486.
7. Cutolo, M., Capellino, S., Sulli, A., Serioli, B., Secchi, M. E., Villaggio, B., and Straub, R. H. (2006). Estrogens and autoimmune diseases. Ann. N. Y. Acad. Sci. 1089, 538-547.
8. Das, C., Kumar, V. S., Gupta, S., and Kumar, S. (2002). Network of cytokines, integrins and hormones in human trophoblast cells. J. Re-prod. Immunol. 53, 257-268.
9. Dore-Duffy, P., Balabanov, R., Washington, R., and Swanborg, R. H. (1994). Transforming growth factor beta 1 inhibits cytokine-induced CNS endothelial cell activation. Mol. Chem. Neuropathol. 22, 161-175
10. Dubal, D. B., Zhu, H., Yu, J., Rau, S. W., Shughrue, P. J., Merchenthaler, I., Kindy, M. S., and Wise, P. M. (2001). Estrogen receptor alpha, not beta, is a critical link in estradiol-mediated protection against brain injury. Proc. Natl. Acad. Sci. U. S. A. 98, 1952-1957.
11. Fan, L., Young, P. R., Barone, F. C., Feuerstein, G. Z., Smith, D. H., and McIntosh, T. K. (1996). Experimental brain injury induces differential expression of tumor necrosis factor-alpha mRNA in the CNS. Brain Res. Mol. Brain. Res. 36, 287-291.
12. Fee, D. B., Sewell, D. L., Andresen, K., Jacques, T. J., Piaskowski, S., Barger, B. A., Hart, M. N., and Fabry, Z. (2004). Traumatic brain injury increases TGF beta RII expression on endothelial cells. Brain Res. 1012, 52-59.
13. Gibson, C. L., Constantin, D., Prior, M. J., Bath, P. M., and Murphy, S. P. (2005). Progesterone suppresses the inflammatory response and nitric oxide synthase-2 expression following cerebral ischemia. Exp. Neu-rol.193, 522-530.
14. Hans, V. H., Kossmann, T., Joller, H., Otto, V., and Morganti-Kossmann, M. C. (1999). Interleukin-6 and its soluble receptor in serum and ce-rebrospinal fluid after cerebral trauma. Neuroreport 10, 409-412.
15. Hatthachote, P., and Gillespie, J. I. (1999). Complex interactions between sex steroids and cytokines in the human pregnant myometrium: evidence for an autocrine signaling system at term. Endocrinology 140, 2533-2540.
16. He, J., Evans, C. O., Hoffman, S. W., Oyesiku, N. M., and Stein, D. G. (2004). Progesterone and allopregnanolone reduce inflammatory cyto-kines after traumatic brain injury. Exp. Neurol. 189, 404-412.
17. Hoffman, G. E., Merchenthaler, I., and Zup, S. L. (2006). Neuroprotection by ovarian hormones in animal models of neurological disease. Endocrine 29, 217-231.
18. Hoffman, S. W., He, J., and Stein, D.G. (2001). Allopregnanolone promotes functional recovery from TBI by reducing cerebral edema and neuronal death. Acad. Emerg. Med. 8, 496-497.
19. Holmin, S., and Hojeberg, B. (2004). In situ detection of intracerebral cyto-kine expression after human brain contusion. Neurosci. Lett. 369, 108-114.
20. Holmin, S., and Mathiesen, T. (2000). Intracerebral administration of in-terleukin-1beta and induction of inflammation, apoptosis, and vasogenic edema. J. Neurosurg. 92, 108-120.
21. Houdeau, E., Moriez, R., Leveque, M., Salvador-Cartier, C., Waget, A., Leng, L., Bueno, L., Bucala, R., and Fioramonti, J. (2007). Sex steroid regulation of macrophage migration inhibitory factor in normal and inflamed colon in the female rat. Gastroenterology 132, 982-993.
22. Hrekova, S. P., Vodianyk, M. O., & Chernyshov, V. P. (2002). Effect of progesterone and 17beta-estradiol on proinflammatory cytokine costi-mulatory proliferative activity. Fiziol. Zh. 48, 63-69.
23. Hussein, M. Z., Al Fikky, A., Abdel Bar, I., and Attia, O. (2004). Serum IL-6 and IL-12 levels in breast cancer patients. Egypt. J. Immunol. 11, 165-170.
24. Jain, S. K., Kannan, K., Prouty, L., and Jain, S. K. (2004). Progesterone, but not 17beta-estradiol, increases TNF-alpha secretion in U937 monocytes. Cytokine 26, 102-105.
25. Jones, N. C., Constantin, D., Prior, M. J., Morris, P. G., Marsden, C. A., and Murphy, S. (2005). The neuroprotective effect of progesterone after traumatic brain injury in male mice is independent of both the inflammatory response and growth factor expression. Eur. J. Neurosci. 21, 1547-1554.
26. Jones, N. C., Prior, M. J., Burden-Teh, E., Marsden, C. A., Morris, P. G., and Murphy, S. (2005). Antagonism of the interleukin-1 receptor following traumatic brain injury in the mouse reduces the number of nitric oxide synthase-2-positive cells and improves anatomical and functional outcomes. Eur. J. Neurosci. 22, 72-78.
27. Jonsson, D. (2007). The biological role of the female sex hormone estrogen in the periodontium-studies on human periodontal ligament cells. Swed. Dent. J. Suppl. 11-54.
28. Konsman, J. P., Drukarch, B., and Van Dam, A. M. (2007). (Peri)vascular production and action of pro-inflammatory cytokines in brain pathology. Clin. Sci. 112, 1-25.
29. Lacut, K., Oger, E., Le Gal, G., Blouch, M. T., Abgrall, J. F., Kerlan, V., Scarabin, P. Y., and Mottier, D. (2003). Differential effects of oral and transdermal postmenopausal estrogen replacement therapies on C-re-active protein. Thromb. Haemost. 90, 124-131.
30. LaMarca, B. D., Chandler, D. L., Grubbs, L., Bain, J., McLemore, G. R., Jr., Granger, J. P., and Ryan, M. J. (2007) Role of sex steroids in modulating tumor necrosis factor alpha-induced changes in vascular function and blood pressure. Am. J. Hypertens. 20, 1216-1221.
31. Lawrence, C. B., Allan, S. M., and Rothwell, N. J. (1998). Interleukin-1beta and the interleukin-1 receptor antagonist act in the striatum to modify excitotoxic brain damage in the rat. Eur. J. Neurosci. 10, 1188-1195.
32. Lenzlinger, P. M., Morganti-Kossmann, M. C., Laurer, H. L., and McIn-tosh, T. K. (2001). The duality of the inflammatory response to traumatic brain injury. Mol. Neurobiol. 24, 169-181.
33. Lu, K. T., Wu, C. Y., Yen, H. H., Peng, J. H., Wang, C. L., and Yang, Y. L. (2007). Bumetanide administration attenuated traumatic brain injury through IL-1 overexpression. Neurol. Res. 29, 404-409.
34. McIntosh, T. K., Juhler, M., and Wieloch, T. (1998). Novel pharmacologic strategies in the treatment of experimental traumatic brain injury. J. Neurotrauma 15, 731-769.
35. Morganti-Kossman, M. C., Lenzlinger, P. M., Hans, V., Stahel, P., Csuka, E., Ammann, E., Stocker, R., Trentz, O., and Kossmann, T. (1997). Production of cytokines following brain injury: beneficial and deleterious for the damaged tissue. Mol. Psychiatry. 2, 133-136.
36. Morganti-Kossmann, M. C., Rancan, M., Stahel, P. F., and Kossmann, T. (2002). Inflammatory response in acute traumatic brain injury: a double-edged sword. Curr. Opin. Crit. Care 8, 101-105.
37. Morrison, B., 3rd, Saatman, K. E., Meaney, D. F., and McIntosh, T. K. (1998). In vitro central nervous system models of mechanically induced trauma: a review. J. Neurotrauma 15, 911-928.
38. O'Connor, C. A., Cernak, I., and Vink, R. (2005). Both estrogen and progesterone attenuate edema formation following diffuse traumatic brain injury in rats. Brain Res. 1062, 171-174.
39. Olsson, T. (1995). Critical influences of the cytokine orchestration on the outcome of myelin antigen-specific T-cell autoimmunity in experimental autoimmune encephalomyelitis and multiple sclerosis. Immunol. Rev. 144, 245-268.
40. Rimaniol, A. C., Lekieffre, D., Serrano, A., Masson, A., Benavides, J., and Zavala, F. (1995). Biphasic transforming growth factor-beta production flanking the pro-inflammatory cytokine response in cerebral trauma. Neuroreport 7, 133-136.
41. Roof, R. L., Duvdevani, R., and Stein, D. G. (1993). Gender influences outcome of brain injury: progesterone plays a protective role. Brain Res, 607, 333-336.
42. Ross, S. A., Halliday, M. I., Campbell, G. C., Byrnes, D. P., and Rowlands, B. J. (1994). The presence of tumour necrosis factor in CSF and plasma after severe head injury. Br. J. Neurosurg. 8, 419-425.
43. Rostworowski, M., Balasingam, V., Chabot, S., Owens, T., and Yong, V. W. (1997). Astrogliosis in the neonatal and adult murine brain post-trauma: elevation of inflammatory cytokines and the lack of requirement for endogenous interferon-gamma. J. Neurosci. 17, 3664-3674
44. Rothwell, N. J., and Hopkins, S. J. (1995). Cytokines and the nervous system II: Actions and mechanisms of action. Trends Neurosci. 18, 130-136.
45. Schaefer, T. M., Wright, J. A., Pioli, P. A., and Wira, C. R. (2005). IL-1beta-mediated proinflammatory responses are inhibited by estradiol via down-regulation of IL-1 receptor type I in uterine epithelial cells. J. Immunol. 175, 6509-6516.
46. Scherbel, U., Raghupathi, R., Nakamura, M., Saatman, K. E., Trojanowski, J. Q., Neugebauer, E., Marino, M. W., and McIntosh, T. K. (1999). Differential acute and chronic responses of tumor necrosis factor-deficient mice to experimental brain injury. Proc. Natl. Acad. Sci. U. S. A. 96, 8721-8726.
47. Shahrokhi, N., Khaksari, M., Soltani, Z., Mahmoodi, M., and Nakhaee, N. (2010). effect of sex steroid hormones on brain edema, intracranial pressure and neurologic outcome after traumatic brain injury. Can. J. Physiol. Pharmacol. 88, 414-421.
48. Shifren, J. L., Rifai, N., Desindes, S., McIlwain, M., Doros, G., and Mazer, N. A. (2008). A comparison of the short-term effects of oral conjugated equine estrogens versus transdermal estradiol on C-reactive protein, other serum markers of inflammation, and other hepatic proteins in naturally menopausal women. J. Clin. Endocrinol. Metab. 93, 1702-171.
49. Shiozaki, T., Hayakata, T., Tasaki, O., Hosotubo, H., Fuijita, K., Mouri, T., Tajima, G., Kajino, K., Nakae, H., Tanaka, H., Shimazu, T., and Su-gimoto, H. (2005). Cerebrospinal fluid concentrations of anti-inflammatory mediators in early-phase severe traumatic brain injury. Shock 23, 406-410.
50. Soltani, Z., Khaksari, M., Shahrokhi, N., Nakhaeei, N., and Shaibani, V. (2009). Effect of Combined Administration of Estrogen and Progesterone on Brain Edema and Neurological Outcome after Traumatic Brain Injury in Female Rats. Iranian Journal of Endocrinology and Metabolism 10, 629-638.
51. Stein, D.G., Wright, D. W., and Kellermann, A.L. (2008). Does progesterone have neuroprotective roperties? Ann. Emerg. Med. 51, 164-172.
52. Streit, W. J., Semple-Rowland, S. L., Hurley, S. D., Miller, R. C., Popo-vich, P. G., and Stokes, B. T. (1998). Cytokine mRNA profiles in contused spinal cord and axotomized facial nucleus suggest a beneficial role for inflammation and gliosis. Exp. Neurol. 152, 74-87.
53. Sullivan, P. G., Bruce-Keller, A. J., Rabchevsky, A. G., Christakos, S., Clair, D. K., Mattson, M. P., and Scheff, S. W. (1999). Exacerbation of damage and altered NF-kappaB activation in mice lacking tumor necrosis factor receptors after traumatic brain injury. J. Neurosci. 19, 6248-6256.
54. Taupin, V., Toulmond, S., Serrano, A., Benavides, J., and Zavala, F. (1993). Increase in IL-6, IL-1 and TNF levels in rat brain following traumatic lesion. Influence of pre-and post-traumatic treatment with Ro5 4864, a peripheral-type (p site) benzodiazepine ligand. J. Neu-roimmunol. 42, 177-185.
55. Won, C. K., Kim, M. O., and Koh, P. O. (2006). Estrogen modulates Bcl-2 family proteins in ischemic brain injury. J. Vet. Med. Sci. 68, 277-280.
56. Woodroofe, M. N., Sarna, G. S., Wadhwa, M., Hayes, G. M., Loughlin, A J., Tinker, A., and Cuzner, M. L. (1991). Detection of interleukin-1 and interleukin-6 in adult rat brain, following mechanical injury, by in vivo microdialysis: evidence of a role for microglia in cytokine production. J. Neuroimmunol. 33, 227-236.
57. Wright, D. W., Bauer, M. E., Hoffman, S. W., and Stein, D. G. (2001). Serum progesterone levels correlate with decreased cerebral edema after traumatic brain injury in male rats. J. Neurotrauma 18, 901-909.
58. Yuan, K., Wing, L. Y., and Lin, M. T. (2002). Pathogenetic roles of angiogenic factors in pyogenic granulomas in pregnancy are modulated by female sex hormones. J. Periodontol. 73, 701-708.