XY sex chromosome complement, compared with XX, in the CNS confers greater neurodegeneration during experimental autoimmune encephalomyelitis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 7, 2014, Pages 2806-2811

  Du, Sienmi ^a,b   Itoh, Noriko ^a   Askarinam, Sahar ^a   Hill, Haley ^a   Arnold, Arthur P ^b   Voskuhl, Rhonda R ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Sex differences; Tlr7; XY genes

Indexed keywords

SEX DIFFERENCES; TLR7; XY GENES;

ANALYSIS OF VARIANCE; ANIMALS; BONE MARROW TRANSPLANTATION; CENTRAL NERVOUS SYSTEM; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; IN SITU HYBRIDIZATION, FLUORESCENCE; MALE; MICE; NERVE DEGENERATION; SEX CHROMOSOMES; TOLL-LIKE RECEPTOR 7; TRANSPLANTATION CHIMERA;

EID: 84894319133     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1307091111     Document Type: Article

References (43)

1. Whitacre CC, Reingold SC, O'Looney PA (1999) A gender gap in autoimmunity. Science 283(5406):1277-1278.
2. Voskuhl RR, Gold SM (2012) Sex-related factors in multiple sclerosis susceptibility and progression. Nat Rev Nephrol 8(5):255-263.
3. Weinshenker BG, et al. (1991) The natural history of multiple sclerosis-A geographically based study. Brain 112(Pt 1):133-146.
4. Weinshenker BG (1994) Natural history of multiple sclerosis. Ann Neurol 36(Suppl): S6-S11.
5. Confavreux C, Vukusic S, Adeleine P (2003) Early clinical predictors and progression of irreversible disability in multiple sclerosis: An amnesic process. Brain 126(Pt 4): 770-782.
6. Pozzilli C, et al. (2003) 'Gender gap' in multiple sclerosis: Magnetic resonance imaging evidence. Eur J Neurol 10(1):95-97.
7. Savettieri G, et al. (2004) Gender-related effect of clinical and genetic variables on the cognitive impairment in multiple sclerosis. J Neurol 251(10):1208-1214.
8. Antulov R, et al. (2009) Gender-related differences in MS: A study of conventional and nonconventional MRI measures. Mult Scler 15(3):345-354.
9. Smith-Bouvier DL, et al. (2008) A role for sex chromosome complement in the female bias in autoimmune disease. J Exp Med 205(5):1099-1108.
10. Nguyen DK, Disteche CM (2006) High expression of the mammalian X chromosome in brain. Brain Res 1126(1):46-49.
11. Gregg C, et al. (2010) High-resolution analysis of parent-of-origin allelic expression in the mouse brain. Science 329(5992):643-648.
12. Carruth LL, Reisert I, Arnold AP (2002) Sex chromosome genes directly affect brain sexual differentiation. Nat Neurosci 5(10):933-934.
13. Luders E, Gaser C, Narr KL, Toga AW (2009) Why sex matters: Brain size independent differences in gray matter distributions between men and women. J Neurosci 29(45): 14265-14270.
14. Spring S, Lerch JP, Henkelman RM (2007) Sexual dimorphism revealed in the structure of the mouse brain using three-dimensional magnetic resonance imaging. Neuroimage 35(4):1424-1433.
15. Dorr AE, Lerch JP, Spring S, Kabani N, Henkelman RM (2008) High resolution threedimensional brain atlas using an average magnetic resonance image of 40 adult C57Bl/6J mice. Neuroimage 42(1):60-69.
16. Cahill L (2006) Why sex matters for neuroscience. Nat Rev Neurosci 7(6):477-484.
17. Paxinos G, Franklin KB (2012) Paxinos and Franklin's the Mouse Brain in Stereotaxic Coordinates (Academic, San Diego), 4th Ed.
18. Rasmussen S, et al. (2007) Persistent activation of microglia is associated with neuronal dysfunction of callosal projecting pathways and multiple sclerosis-like lesions in relapsing-remitting experimental autoimmune encephalomyelitis. Brain 130(Pt 11): 2816-2829.
19. MacKenzie-Graham A, et al. (2012) Cortical atrophy in experimental autoimmune encephalomyelitis: In vivo imaging. Neuroimage 60(1):95-104.
20. Ziehn MO, et al. (2012) Therapeutic testosterone administration preserves excitatory synaptic transmission in the hippocampus during autoimmune demyelinating disease. J Neurosci 32(36):12312-12324.
21. Ziehn MO, Avedisian AA, Dervin SM, O'Dell TJ, Voskuhl RR (2012) Estriol preserves synaptic transmission in the hippocampus during autoimmune demyelinating disease. Lab Invest 92(8):1234-1245.
22. Lehmann SM, et al. (2012) An unconventional role for miRNA: Let-7 activates Toll-like receptor 7 and causes neurodegeneration. Nat Neurosci 15(6):827-835.
23. Usdin MT, Shelbourne PF, Myers RM, Madison DV (1999) Impaired synaptic plasticity in mice carrying the Huntington's disease mutation. Hum Mol Genet 8(5):839-846.
24. Masliah E, et al. (2001) Altered expression of synaptic proteins occurs early during progression of Alzheimer's disease. Neurology 56(1):127-129.
25. Wise PM (2002) Estrogens and neuroprotection. Trends Endocrinol Metab 13(6): 229-230.
26. Pike CJ, Carroll JC, Rosario ER, Barron AM (2009) Protective actions of sex steroid hormones in Alzheimer's disease. Front Neuroendocrinol 30(2):239-258.
27. Bourque M, Dluzen DE, Di Paolo T (2009) Neuroprotective actions of sex steroids in Parkinson's disease. Front Neuroendocrinol 30(2):142-157.
28. Spence RD, Voskuhl RR (2012) Neuroprotective effects of estrogens and androgens in CNS inflammation and neurodegeneration. Front Neuroendocrinol 33(1):105-115.
29. Matejuk A, et al. (2001) 17 beta-estradiol inhibits cytokine, chemokine, and chemokine receptor mRNA expression in the central nervous system of female mice with experimental autoimmune encephalomyelitis. J Neurosci Res 65(6):529-542.
30. Voskuhl RR, Palaszynski K (2001) Sex hormones in experimental autoimmune encephalomyelitis: Implications for multiple sclerosis. Neuroscientist 7(3):258-270.
31. Jansson L, Olsson T, Holmdahl R (1994) Estrogen induces a potent suppression of experimental autoimmune encephalomyelitis and collagen-induced arthritis in mice. J Neuroimmunol 53(2):203-207.
32. Kim S, Dalal M, Voskuhl R (1998) Estriol ameliorates EAE: Mechanisms in the shift toward Th2 during pregnancy. Neurology 50(4):A424-A425.
33. Palaszynski KM, Loo KK, Ashouri JF, Liu HB, Voskuhl RR (2004) Androgens are protective in experimental autoimmune encephalomyelitis: Implications for multiple sclerosis. J Neuroimmunol 146(1-2):144-152.
34. Hussain R, et al. (2013) The neural androgen receptor: A therapeutic target for myelin repair in chronic demyelination. Brain 136(Pt 1):132-146.
35. Palaszynski KM, et al. (2005) A yin-yang effect between sex chromosome complement and sex hormones on the immune response. Endocrinology 146(8):3280-3285.
36. De Vries GJ (2004) Minireview: Sex differences in adult and developing brains: Compensation, compensation, compensation. Endocrinology 145(3):1063-1068.
37. Burgoyne PS (1998) The role of Y-encoded genes in mammalian spermatogenesis. Semin Cell Dev Biol 9(4):423-432.
38. Arnold AP, Chen X, Link JC, Itoh Y, Reue K (2013) Cell-autonomous sex determination outside of the gonad. Dev Dyn 242(4):371-379.
39. Arnold AP (2009) Mouse models for evaluating sex chromosome effects that cause sex differences in non-gonadal tissues. J Neuroendocrinol 21(4):377-386.
40. Davies W, Isles AR, Humby T, Wilkinson LS (2007) What are imprinted genes doing in the brain? Epigenetics 2(4):201-206.
41. Davies W, et al. (2005) Xlr3b is a new imprinted candidate for X-linked parent-oforigin effects on cognitive function in mice. Nat Genet 37(6):625-629.
42. Arnold AP, Burgoyne PS (2004) Are XX and XY brain cells intrinsically different? Trends Endocrinol Metab 15(1):6-11.
43. Du S, Sandoval F, Trinh P, Voskuhl RR (2010) Additive effects of combination treatment with anti-inflammatory and neuroprotective agents in experimental autoimmune encephalomyelitis. J Neuroimmunol 219(1-2):64-74.