17β-Estradiol protects Schwann cells against H2O2-induced cytotoxicity and increases transplanted Schwann cell survival in a cervical hemicontusion spinal cord injury model

Journal of Neurochemistry

Volumn 115, Issue 4, 2010, Pages 864-872

  Siriphorn, Akkradate ^a,b   Chompoopong, Supin ^b   Floyd, Candace L ^a  

^a University of Alabama at Birmingham   (United States)

^b MAHIDOL UNIVERSITY   (Thailand)

Author keywords

Cell transplantation; Cervical; Estrogen; Oxidative injury; Schwann cell; Spinal cord injury

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR; FULVESTRANT; HYDROGEN PEROXIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DEATH; CELL PROTECTION; CELL SURVIVAL; CELL TRANSPLANTATION; CERVICAL SPINAL CORD INJURY; COMPETITIVE INHIBITION; CONTROLLED STUDY; CYTOTOXICITY; DOSE RESPONSE; IN VITRO STUDY; MALE; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SCHWANN CELL; SIGNAL TRANSDUCTION;

ANIMALS; ANIMALS, NEWBORN; CELL SURVIVAL; CELL TRANSPLANTATION; CERVICAL VERTEBRAE; CYTOTOXINS; ESTRADIOL; HYDROGEN PEROXIDE; MALE; NEUROPROTECTIVE AGENTS; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; SCHWANN CELLS; SPINAL CORD INJURIES;

RATTUS;

EID: 77958543505     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.06770.x     Document Type: Article

References (64)

1. Akiyama Y., Lankford K., Radtke C., Greer C. A. and Kocsis J. D. (2004) Remyelination of spinal cord axons by olfactory ensheathing cells and Schwann cells derived from a transgenic rat expressing alkaline phosphatase marker gene. Neuron Glia Biol. 1, 47-55.
2. Askwith T., Zeng W., Eggo M. C. and Stevens M. J. (2009) Oxidative stress and dysregulation of the taurine transporter in high-glucose-exposed human Schwann cells: implications for pathogenesis of diabetic neuropathy. Am. J. Physiol. Endocrinol. Metab. 297, E620-E628.
3. Bachelin C., Lachapelle F., Girard C. et al. (2005) Efficient myelin repair in the macaque spinal cord by autologous grafts of Schwann cells. Brain 128, 540-549.
4. Baek S. Y. and Kim S. U. (1998) Proliferation of human Schwann cells induced by neu differentiation factor isoforms. Dev. Neurosci. 20, 512-517.
5. Ban D. X., Kong X. H., Feng S. Q., Ning G. Z., Chen J. T. and Guo S. F. (2009) Intraspinal cord graft of autologous activated Schwann cells efficiently promotes axonal regeneration and functional recovery after rat's spinal cord injury. Brain Res. 1256, 149-161.
6. Behl C. (2002) Oestrogen as a neuroprotective hormone. Nat. Rev. Neurosci. 3, 433-442.
7. Behl C., Widmann M., Trapp T. and Holsboer F. (1995) 17-beta estradiol protects neurons from oxidative stress-induced cell death in vitro. Biochem. Biophys. Res. Commun. 216, 473-482.
8. Behl C., Skutella T., Lezoualc'h F., Post A., Widmann M., Newton C. J. and Holsboer F. (1997) Neuroprotection against oxidative stress by estrogens: structure-activity relationship. Mol. Pharmacol. 51, 535-541.
9. Biewenga E., Cabell L. and Audesirk T. (2005) Estradiol and raloxifene protect cultured SN4741 neurons against oxidative stress. Neurosci. Lett. 373, 179-183.
10. Brockes J. P., Fields K. L. and Raff M. C. (1979) Studies on cultured rat Schwann cells. I. Establishment of purified populations from cultures of peripheral nerve. Brain Res. 165, 105-118.
11. Cameron N. E. and Cotter M. A. (1999) Effects of antioxidants on nerve and vascular dysfunction in experimental diabetes. Diabetes Res. Clin. Pract. 45, 137-146.
12. Cao Q., Xu X. M., DeVries W. H., Enzmann G. U., Ping P., Tsoulfas P., Wood P. M., Bunge M. B. and Whittemore S. R. (2005) Functional recovery in traumatic spinal cord injury after transplantation of multineurotrophin-expressing glial-restricted precursor cells. J. Neurosci. 25, 6947-6957.
13. Chaovipoch P., Jelks K. A., Gerhold L. M., West E. J., Chongthammakun S. and Floyd C. L. (2006) 17beta-estradiol is protective in spinal cord injury in post- and pre-menopausal rats. J. Neurotrauma 23, 830-852.
14. Crossthwaite A. J., Hasan S. and Williams R. J. (2002) Hydrogen peroxide-mediated phosphorylation of ERK1/2, Akt/PKB and JNK in cortical neurones: dependence on Ca(2+) and PI3-kinase. J. Neurochem. 80, 24-35.
15. Cuzzocrea S., Genovese T., Mazzon E., Esposito E., Di P. R., Muia C., Crisafulli C., Peli A., Bramanti P. and Chaudry I. H. (2008) Effect of 17beta-estradiol on signal transduction pathways and secondary damage in experimental spinal cord trauma. Shock 29, 362-371.
16. Dinh P., Bhatia N., Rasouli A., Suryadevara S., Cahill K. and Gupta R. (2007) Transplantation of preconditioned Schwann cells following hemisection spinal cord injury. Spine (Phila Pa 1976.) 32, 943-949.
17. Eckersley L. (2002) Role of the Schwann cell in diabetic neuropathy. Int. Rev. Neurobiol. 50, 293-321.
18. Eftekharpour E., Karimi-Abdolrezaee S. and Fehlings M. G. (2008) Current status of experimental cell replacement approaches to spinal cord injury. Neurosurg. Focus. 24, E19.
19. Fishbein L., Zhang X., Fisher L. B., Li H., Campbell-Thompson M., Yachnis A., Rubenstein A., Muir D. and Wallace M. R. (2007) In vitro studies of steroid hormones in neurofibromatosis 1 tumors and Schwann cells. Mol. Carcinog. 46, 512-523.
20. Fortun J., Hill C. E. and Bunge M. B. (2009) Combinatorial strategies with Schwann cell transplantation to improve repair of the injured spinal cord. Neurosci. Lett. 456, 124-132.
21. Funakoshi H., Frisen J., Barbany G., Timmusk T., Zachrisson O., Verge V. M. and Persson H. (1993) Differential expression of mRNAs for neurotrophins and their receptors after axotomy of the sciatic nerve. J. Cell Biol. 123, 455-465.
22. Golden K. L., Pearse D. D., Blits B., Garg M. S., Oudega M., Wood P. M. and Bunge M. B. (2007) Transduced Schwann cells promote axon growth and myelination after spinal cord injury. Exp. Neurol. 207, 203-217.
23. Haastert K., Mauritz C., Chaturvedi S. and Grothe C. (2007) Human and rat adult Schwann cell cultures: fast and efficient enrichment and highly effective non-viral transfection protocol. Nat. Protoc. 2, 99-104.
24. Hall E. D. and Springer J. E. (2004) Neuroprotection and acute spinal cord injury: a reappraisal. NeuroRx 1, 80-100.
25. Hendricks W. A., Pak E. S., Owensby J. P., Menta K. J., Glazova M., Moretto J., Hollis S., Brewer K. L. and Murashov A. K. (2006) Predifferentiated embryonic stem cells prevent chronic pain behaviors and restore sensory function following spinal cord injury in mice. Mol. Med. 12, 34-46.
26. Hill C. E., Moon L. D., Wood P. M. and Bunge M. B. (2006) Labeled Schwann cell transplantation: cell loss, host Schwann cell replacement, and strategies to enhance survival. Glia 53, 338-343.
27. Hill C. E., Hurtado A., Blits B., Bahr B. A., Wood P. M., Bartlett B. M. and Oudega M. (2007) Early necrosis and apoptosis of Schwann cells transplanted into the injured rat spinal cord. Eur. J. Neurosci. 26, 1433-1445.
28. Kachadroka S., Hall A. M., Niedzielko T. L., Chongthammakun S. and Floyd C. L. (2010) Effect of endogenous androgens on 17b-estradiol-mediated protection after spinal cord injury in male rats. J. Neurotrauma 27, 611-626.
29. Kanda N. and Watanabe S. (2003) 17beta-estradiol inhibits oxidative stress-induced apoptosis in keratinocytes by promoting Bcl-2 expression. J. Invest. Dermatol. 121, 1500-1509.
30. Keirstead H. S., Nistor G., Bernal G., Totoiu M., Cloutier F., Sharp K. and Steward O. (2005) Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J. Neurosci. 25, 4694-4705.
31. Kocsis J. D., Lankford K. L., Sasaki M. and Radtke C. (2009) Unique in vivo properties of olfactory ensheathing cells that may contribute to neural repair and protection following spinal cord injury. Neurosci. Lett. 456, 137-142.
32. Kwon B. K., Tetzlaff W., Grauer J. N., Beiner J. and Vaccaro A. R. (2004) Pathophysiology and pharmacologic treatment of acute spinal cord injury. Spine J. 4, 451-464.
33. Lavdas A. A., Chen J., Papastefanaki F., Chen S., Schachner M., Matsas R. and Thomaidou D. (2010) Schwann cells engineered to express the cell adhesion molecule L1 accelerate myelination and motor recovery after spinal cord injury. Exp. Neurol. 221, 206-216.
34. Li X., Dancausse H., Grijalva I., Oliveira M. and Levi A. D. (2003) Labeling Schwann cells with CFSE-an in vitro and in vivo study. J. Neurosci. Methods 125, 83-91.
35. Liu D., Liu J. and Wen J. (1999) Elevation of hydrogen peroxide after spinal cord injury detected by using the Fenton reaction. Free Radic. Biol. Med. 27, 478-482.
36. Meyer M., Matsuoka I., Wetmore C., Olson L. and Thoenen H. (1992) Enhanced synthesis of brain-derived neurotrophic factor in the lesioned peripheral nerve: different mechanisms are responsible for the regulation of BDNF and NGF mRNA. J. Cell Biol. 119, 45-54.
37. Munoz-Quiles C., Santos-Benito F. F., Llamusi M. B. and Ramon-Cueto A. (2009) Chronic spinal injury repair by olfactory bulb ensheathing glia and feasibility for autologous therapy. J. Neuropathol. Exp. Neurol. 68, 1294-1308.
38. Numakawa Y., Matsumoto T., Yokomaku D., Taguchi T., Niki E., Hatanaka H., Kunugi H. and Numakawa T. (2007) 17beta-estradiol protects cortical neurons against oxidative stress-induced cell death through reduction in the activity of mitogen-activated protein kinase and in the accumulation of intracellular calcium. Endocrinology 148, 627-637.
39. Onose G., Anghelescu A., Muresanu D. F. et al. (2009) A review of published reports on neuroprotection in spinal cord injury. Spinal Cord 47, 716-726.
40. Oudega M., Moon L. D. and De Almeida Leme R. J. (2005) Schwann cells for spinal cord repair. Braz. J. Med. Biol. Res. 38, 825-835.
41. Papastefanaki F., Chen J., Lavdas A. A., Thomaidou D., Schachner M. and Matsas R. (2007) Grafts of Schwann cells engineered to express PSA-NCAM promote functional recovery after spinal cord injury. Brain 130, 2159-2174.
42. Patel A. K., Alexander T. H., Andalibi A., Ryan A. F. and Doherty J. K. (2008) Vestibular schwannoma quantitative polymerase chain reaction expression of estrogen and progesterone receptors. Laryngoscope 118, 1458-1463.
43. Pearse D. D., Sanchez A. R., Pereira F. C. et al. (2007) Transplantation of Schwann cells and/or olfactory ensheathing glia into the contused spinal cord: survival, migration, axon association, and functional recovery. Glia 55, 976-1000.
44. Pizzi M. A. and Crowe M. J. (2006) Transplantation of fibroblasts that overexpress matrix metalloproteinase-3 into the site of spinal cord injury in rats. J. Neurotrauma 23, 1750-1765.
45. Prokai L. and Simpkins J. W. (2007) Structure-nongenomic neuroprotection relationship of estrogens and estrogen-derived compounds. Pharmacol. Ther. 114, 1-12.
46. Raz L., Khan M. M., Mahesh V. B., Vadlamudi R. K. and Brann D. W. (2008) Rapid estrogen signaling in the brain. Neurosignals 16, 140-153.
47. Setoguchi T., Nakashima K., Takizawa T., Yanagisawa M., Ochiai W., Okabe M., Yone K., Komiya S. and Taga T. (2004) Treatment of spinal cord injury by transplantation of fetal neural precursor cells engineered to express BMP inhibitor. Exp. Neurol. 189, 33-44.
48. Kay-Sim A., Feron F., Cochrane J. et al. (2008) Autologous olfactory ensheathing cell transplantation in human paraplegia: a 3-year clinical trial. Brain 131, 2376-2386.
49. Simpkins J. W. and Dykens J. A. (2008) Mitochondrial mechanisms of estrogen neuroprotection. Brain Res. Rev. 57, 421-430.
50. Singh M., Dykens J. A. and Simpkins J. W. (2006) Novel mechanisms for estrogen-induced neuroprotection. Exp. Biol. Med. (Maywood.) 231, 514-521.
51. Sribnick E. A., Wingrave J. M., Matzelle D. D., Wilford G. G., Ray S. K. and Banik N. L. (2005) Estrogen attenuated markers of inflammation and decreased lesion volume in acute spinal cord injury in rats. J. Neurosci. Res. 82, 283-293.
52. Sribnick E. A., Matzelle D. D., Ray S. K. and Banik N. L. (2006) Estrogen treatment of spinal cord injury attenuates calpain activation and apoptosis. J. Neurosci. Res. 84, 1064-1075.
53. Sur P., Sribnick E. A., Wingrave J. M., Nowak M. W., Ray S. K. and Banik N. L. (2003) Estrogen attenuates oxidative stress-induced apoptosis in C6 glial cells. Brain Res. 971, 178-188.
54. Takami T., Oudega M., Bates M. L., Wood P. M., Kleitman N. and Bunge M. B. (2002) Schwann cell but not olfactory ensheathing glia transplants improve hindlimb locomotor performance in the moderately contused adult rat thoracic spinal cord. J. Neurosci. 22, 6670-6681.
55. Takao T., Flint N., Lee L., Ying X., Merrill J. and Chandross K. J. (2004) 17beta-estradiol protects oligodendrocytes from cytotoxicity induced cell death. J. Neurochem. 89, 660-673.
56. Taylor J. S. and Bampton E. T. (2004) Factors secreted by Schwann cells stimulate the regeneration of neonatal retinal ganglion cells. J. Anat. 204, 25-31.
57. Thuret S., Moon L. D. and Gage F. H. (2006) Therapeutic interventions after spinal cord injury. Nat. Rev. Neurosci. 7, 628-643.
58. Tobias C. A., Han S. S., Shumsky J. S., Kim D., Tumolo M., Dhoot N. O., Wheatley M. A., Fischer I., Tessler A. and Murray M. (2005) Alginate encapsulated BDNF-producing fibroblast grafts permit recovery of function after spinal cord injury in the absence of immune suppression. J. Neurotrauma 22, 138-156.
59. Urata Y., Ihara Y., Murata H., Goto S., Koji T., Yodoi J., Inoue S. and Kondo T. (2006) 17Beta-estradiol protects against oxidative stress-induced cell death through the glutathione/glutaredoxin-dependent redox regulation of Akt in myocardiac H9c2 cells. J. Biol. Chem. 281, 13092-13102.
60. Wang Y., Schmeichel A. M., Iida H., Schmelzer J. D. and Low P. A. (2005) Ischemia-reperfusion injury causes oxidative stress and apoptosis of Schwann cell in acute and chronic experimental diabetic neuropathy. Antioxid. Redox Signal. 7, 1513-1520.
61. Wang X., Dykens J. A., Perez E., Liu R., Yang S., Covey D. F. and Simpkins J. W. (2006) Neuroprotective effects of 17beta-estradiol and nonfeminizing estrogens against H2O2 toxicity in human neuroblastoma SK-N-SH cells. Mol. Pharmacol. 70, 395-404.
62. Winterle J. S., Mill T., Harris T. and Goldbeck R. A. (2001) Absolute kinetic characterization of 17-beta-estradiol as a radical-scavenging, antioxidant synergist. Arch. Biochem. Biophys. 392, 233-244.
63. Yu X., Rajala R. V., McGinnis J. F. et al. (2004) Involvement of insulin/phosphoinositide 3-kinase/Akt signal pathway in 17 beta-estradiol-mediated neuroprotection. J. Biol. Chem. 279, 13086-13094.
64. Ziv Y., Avidan H., Pluchino S., Martino G. and Schwartz M. (2006) Synergy between immune cells and adult neural stem/progenitor cells promotes functional recovery from spinal cord injury. Proc. Natl Acad. Sci. USA 103, 13174-13179.