Inhibition of Autophagy by Estradiol Promotes Locomotor Recovery after Spinal Cord Injury in Rats

Neuroscience Bulletin

Volumn 32, Issue 2, 2016, Pages 137-144

  Lin, Chao Wei ^a   Chen, Bi ^a   Huang, Ke Lun ^a   Dai, Yu Sen ^a   Teng, Hong Lin ^a  

^a THE FIRST AFFILIATED HOSPITAL OF WENZHOU MEDICAL UNIVERSITY   (China)

Author keywords

17 estradiol; Autophagy; Motor neuron; Spinal cord injury

Indexed keywords

BECLIN 1; ESTRADIOL; ESTRADIOL BENZOATE; PROTEIN; PROTEIN LC3II; RAPAMYCIN; UNCLASSIFIED DRUG; ESTROGEN; HYDROGEN PEROXIDE; LC3 PROTEIN, RAT; MICROTUBULE ASSOCIATED PROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CELL LOSS; CONTROLLED STUDY; DOWN REGULATION; FEMALE; HORMONE BLOOD LEVEL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN VITRO STUDY; IN VIVO STUDY; LOCOMOTION; MOTONEURON; NEUROPROTECTION; NONHUMAN; PC12 CELL LINE; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SPINAL CORD INJURY; WESTERN BLOTTING; ANIMAL; BLOOD; CONVALESCENCE; DISEASE MODEL; DRUG EFFECTS; FOLLOW UP; GENETICS; METABOLISM; OVARIECTOMY; PATHOLOGY; SPINAL CORD INJURIES; SPRAGUE DAWLEY RAT;

ANIMALS; AUTOPHAGY; BECLIN-1; DISEASE MODELS, ANIMAL; DOWN-REGULATION; ESTRADIOL; ESTROGENS; FEMALE; FOLLOW-UP STUDIES; HYDROGEN PEROXIDE; LOCOMOTION; MICROTUBULE-ASSOCIATED PROTEINS; MOTOR NEURONS; OVARIECTOMY; PC12 CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; SPINAL CORD INJURIES;

EID: 84962747174     PISSN: 16737067     EISSN: 19958218     Source Type: Journal    
DOI: 10.1007/s12264-016-0017-x     Document Type: Article

References (38)

1. Silva NA, Sousa N, Reis RL, Salgado AJ. From basics to clinical: A comprehensive review on spinal cord injury. Prog Neurobiol 2014, 114: 25–57.
2. Suzuki S, Brown CM, Wise PM. Neuroprotective effects of estrogens following ischemic stroke. Front Neuroendocrinol 2009, 30: 201–211.
3. Hoffman GE, Merchenthaler I, Zup SL. Neuroprotection by ovarian hormones in animal models of neurological disease. Endocrine 2006, 29: 217–231.
4. Arevalo MA, Azcoitia I, Garcia-Segura LM. The neuroprotective actions of oestradiol and oestrogen receptors. Nat Rev Neurosci 2015, 16: 17–29.
5. Khaksari M, Abbasloo E, Dehghan F, Soltani Z, Asadikaram G. The brain cytokine levels are modulated by estrogen following traumatic brain injury: Which estrogen receptor serves as modulator? Int Immunopharmacol 2015, 28: 279–287.
6. Webb AA, Chan CB, Brown A, Saleh TM. Estrogen reduces the severity of autonomic dysfunction in spinal cord-injured male mice. Behav Brain Res 2006, 171: 338–49.
7. Ritz MF, Hausmann ON. Effect of 17β-estradiol on functional outcome, release of cytokines, astrocyte reactivity and inflammatory spreading after spinal cord injury in male rats. Brain Res 2008, 1203: 177–188.
8. Guptarak J, Wiktorowicz JE, Sadygov RG, Zivadinovic D, Paulucci-Holthauzen AA, Vergara L. The cancer drug tamoxifen: A potential therapeutic treatment for spinal cord injury. J Neurotrauma 2014, 31: 268–283.
9. Mehta SH, Dhandapani KM, De Sevilla LM, Webb RC, Mahesh VB, Brann DW. Tamoxifen, a selective estrogen receptor modulator, reduces ischemic damage caused by middle cerebral artery occlusion in the ovariectomized female rat. Neuroendocrinology 2003, 77: 44–50.
10. Nikoletopoulou V, Papandreou ME, Tavernarakis N. Autophagy in the physiology and pathology of the central nervous system. Cell Death Differ 2015, 22: 398–407.
11. Wang ZY, Lin JH, Muharram A, Liu WG. Beclin-1-mediated autophagy protects spinal cord neurons against mechanical injury-induced apoptosis. Apoptosis 2014, 19: 933–945.
12. Kanno H, Ozawa H, Sekiguchi A, Yamaya S, Itoi E. Induction of autophagy and autophagic cell death in damaged neural tissue after acute spinal cord injury in mice. Spine (Phila Pa 1976) 2011, 36: E1427–E1434.
13. Zeng M, Chen B, Qing Y, Xie W, Dang W, Zhao M, et al. Estrogen receptor β signaling induces autophagy and downregulates Glut9 expression. Nucleosides Nucleotides Nucleic Acids 2014, 33: 455–465.
14. Mosquera L, Colón JM, Santiago JM, Torrado AI, Meléndez M, Segarra AC, et al. Tamoxifen and estradiol improved locomotor function and increased spared tissue in rats after spinal cord injury: Their antioxidant effect and role of estrogen receptor alpha. Brain Res 2014, 1561: 11–22.
15. Ma YL, Qin P, Li Y, Shen L, Wang SQ, Dong HL, et al. The effects of different doses of estradiol (E2) on cerebral ischemia in an in vitro model of oxygen and glucose deprivation and reperfusion and in a rat model of middle carotid artery occlusion. BMC Neurosci 2013, 14: 118.
16. Yang Y, Zheng X, Li B, et al. Increased activity of osteocyte autophagy in ovariectomized rats and its correlation with oxidative stress status and bone loss. Biochem Biophys Res Commun 2014, 451: 86–92.
17. Beattie MS, Farooqui AA, Bresnahan JC. Review of current evidence for apoptosis after spinal cord injury. J Neurotrauma 2000, 17: 915–925.
18. Yong C, Arnold PM, Zoubine MN, Citron BA, Watanabe I, Berman NE, et al. Apoptosis in cellular compartments of rat spinal cord after severe contusion injury. J Neurotrauma 1998, 15: 459–472.
19. Bjorkoy G, Lamark T, Brech A, Outzen H, Perander M, Overvatn A, et al. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 2005, 171: 603–614.
20. Mathew R, Karp CM, Beaudoin B, Vuong N, Chen G, Chen HY, et al. Autophagy suppresses tumorigenesis through elimination of p62. Cell 2009, 137: 1062–1075.
21. Penas C, Guzman MS, Verdu E, Fores J, Navarro X, Casas C. Spinal cord injury induces endoplasmic reticulum stress with different cell-type dependent response. J Neurochem 2007, 102: 1242–1255.
22. Cevikbas F, Steinhoff M, Ikoma A. Role of spinal neurotransmitter receptors in itch: New insights into therapies and drug development. CNS Neurosci Ther 2011, 17: 742–749.
23. Moon YJ, Lee JY, Oh MS, Pak YK, Park KS, Oh TH, et al. Inhibition of inflammation and oxidative stress by Angelica dahuricae radix extract decreases apoptotic cell death and improves functional recovery after spinal cord injury. J Neurosci Res 2012, 90: 243–256.
24. Chen CW, Chen TY, Tsai KL, Lin CL, Yokoyama KK, Lee WS, et al. Inhibition of autophagy as a therapeutic strategy of iron-induced brain injury after hemorrhage. Autophagy 2012, 8: 1510–1520.
25. Azcoitia I, Arevalo MA, De Nicola AF, Garcia-Segura LM. Neuroprotective actions of estradiol revisited. Trends Endocrinol Metab 2011, 22: 467–473.
26. Hao HH, Wang L, Guo ZJ, Bai L, Zhang RP, Shuang WB, et al. Valproic acid reduces autophagy and promotes functional recovery after spinal cord injury in rats. Neurosci Bull 2013, 29: 484–492.
27. Tang P, Hou H, Zhang L, Lan X, Mao Z, Liu D, et al. Autophagy reduces neuronal damage and promotes locomotor recovery via inhibition of apoptosis after spinal cord injury in rats. Mol Neurobiol. 2014, 49: 276–287.
28. Kanno H, Ozawa H, Sekiguchi A, Itoi E. Spinal cord injury induces upregulation of Beclin 1 and promotes autophagic cell death. Neurobiol Dis 2009, 33: 143–148.
29. Button RW, Luo S, Rubinsztein DC. Autophagic activity in neuronal cell death. Neurosci Bull 2015, 31: 382–394.
30. Sribnick EA, Matzelle DD, Ray SK, Banik NL. Estrogen treatment of spinal cord injury attenuates calpain activation and apoptosis. J Neurosci Res 2006, 84: 1064–1075.
31. Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell 2010, 140: 313–326.
32. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008, 4: 151–175.
33. Brown KN, Chen S, Han Z, Lu CH, Tan X, Zhang XJ, et al. Clonal production and organization of inhibitory interneurons in the neocortex. Science 2011, 334: 480–486.
34. Yang YH, Chen K, Li B, Chen JW, Zheng XF, Wang YR, et al. Estradiol inhibits osteoblast apoptosis via promotion of autophagy through the ER-ERK-mTOR pathway. Apoptosis 2013, 18: 1363–1375.
35. Vanderhorst VG, Gustafsson JA, Ulfhake B. Estrogen receptor-alpha and -beta immunoreactive neurons in the brainstem and spinal cord of male and female mice: Relationships to monoaminergic, cholinergic, and spinal projection systems. J Comp Neurol 2005, 488: 152–179.
36. Hu R1, Sun H, Zhang Q, Chen J, Wu N, Meng H et al. G-protein coupled estrogen receptor 1 mediated estrogenic neuroprotection against spinal cord injury. Crit Care Med 2012, 40: 3230–3237.
37. Vivacqua A, Bonofiglio D, Albanito L, Madeo A, Rago V, Carpino A, et al. 17beta-estradiol, genistein, and 4-hydroxytamoxifen induce the proliferation of thyroid cancer cells through the g protein-coupled receptor GPR30. Mol Pharmacol 2006, 70: 1414–1423.
38. Chen J, Hu R, Ge H, Duanmu W, Li Y, Xue X, et al. G-protein-coupled receptor 30-mediated antiapoptotic effect of estrogen on spinal motor neurons following injury and its underlying mechanisms. Mol Med Rep 2015, 12: 1733–1740.