Impact of aromatase genetic variation on hormone levels and global outcome after severe TBI

Journal of Neurotrauma

Volumn 30, Issue 16, 2013, Pages 1415-1425

  Garringer, Julie A ^a   Niyonkuru, Christian ^a   McCullough, Emily H ^a,b   Loucks, Tammy ^d   Dixon, C Edward ^a,b   Conley, Yvette P ^c   Berga, Sarah ^e   Wagner, Amy K ^a,b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c UNIVERSITY OF PITTSBURGH   (United States)

^d EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

aromatase; estradiol; genetics CYP19A1; testosterone; traumatic brain injury

Indexed keywords

AROMATASE; CITICOLINE; ESTRADIOL; PLACEBO; TESTOSTERONE;

ADULT; AGE; ALLELE; ARTICLE; BLOOD SAMPLING; BODY MASS; CEREBROSPINAL FLUID ANALYSIS; CONTROLLED STUDY; ESTRADIOL BLOOD LEVEL; FEMALE; GENDER; GENETIC ASSOCIATION; GENETIC RISK; GLASGOW OUTCOME SCALE; HUMAN; HUMAN TISSUE; INJURY SEVERITY; MAJOR CLINICAL STUDY; MALE; MORTALITY; MULTICENTER STUDY (TOPIC); PROTEIN CEREBROSPINAL FLUID LEVEL; RANDOMIZED CONTROLLED TRIAL (TOPIC); RISK ASSESSMENT; SINGLE NUCLEOTIDE POLYMORPHISM; TESTOSTERONE BLOOD LEVEL; TRAUMATIC BRAIN INJURY;

ADULT; AROMATASE; BIOLOGICAL MARKERS; BRAIN INJURIES; ESTRADIOL; FEMALE; GENETIC VARIATION; HUMANS; MALE; MIDDLE AGED; POLYMORPHISM, SINGLE NUCLEOTIDE; SEVERITY OF ILLNESS INDEX; TESTOSTERONE; YOUNG ADULT;

EID: 84881449078     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2012.2565     Document Type: Article

References (48)

1. Azcoitia, I., Yague, J.G., and Garcia-Segura, L.M. (2011). Estradiol synthesis within the human brain. Neuroscience 191, 139-347.
2. Arevalo, M.A., Santos-Galindo, M., Bellini, M.J., Azcoitia, I., and Garcia-Segura, L.M. (2010). Actions of estrogens on glial cells: implications for neuroprotection. Biochim. Biophys. Acta. 1800, 1106-1112.
3. Simpson, E.R. (2004). Aromatase: biologic relevance of tissue-specific expression. Semin. Reprod. Med. 22, 11-23. (Pubitemid 38524580)
4. Hojo, Y., Murakami, G., Mukai, H., Higo, S., Hatanaka, Y., Ogiue-Ikeda, M., Ishii, H., Kimoto, T., and Kawato, S. (2008). Estrogen synthesis in the brain-role in synaptic plasticity and memory. Mol. Cell. Endocrinol. 290, 31-43.
5. Bulun, S.E., Takayama, K., Suzuki, T., Sasano, H., Yilmaz, B., and Sebastian, S. (2004). Organization of the human aromatase p450 (CYP19) gene. Semin. Reprod. Med. 22, 5-9. (Pubitemid 38524579)
6. Honda, S., Harada, N., and Takagi, Y. (1994). Novel exon 1 of the aromatase gene specific for aromatase transcripts in human brain. Biochem. Biophys. Res. Commun. 198, 1153-1160. (Pubitemid 24172817)
7. Sebastian, S., and Bulun, S.E. (2001). A highly complex organization of the regulatory region of the human CYP19 (aromatase) gene revealed by the human genome project. J. Clin. Endocrinol. Metab. 86, 4600-4602. (Pubitemid 33020491)
8. Prange-Kiel, J., and Rune, G.M. (2006). Direct and indirect effects of estrogen on rat hippocampus. Neuroscience 138, 765-772.
9. Roof, R.L., and Hall, E.D. (2000). Gender differences in acute CNS trauma and stroke: neuroprotective effects of estrogen and progesterone. J. Neurotrauma 17, 367-388. (Pubitemid 30327300)
10. Wagner, A.K., McCullough, E.H., Niyonkuru, C., Ozawa, H., Loucks, T.L., Dobos, J.A., Brett, C.A., Santarsieri, M., Dixon, C.E., Berga, S.L., and Fabio, A. (2011). Acute serum hormone levels: characterization and prognosis after severe traumatic brain injury. J. Neurotrauma 28, 871-888.
11. MacLusky, N.J., Hajszan, T., Prange-Kiel, J., and Leranth, C. (2006). Androgen modulation of hippocampal synaptic plasticity. Neuroscience 138, 957-965.
12. Herson, P.S., Koerner, I.P., and Hurn, P.D. (2009). Sex, sex steroids, and brain injury. Semin. Reprod. Med. 27, 229-239.
13. Wagner, A.K., Brett, C.A., McCullough, E.H., Niyonkuru, C., Loucks, T.L., Dixon, C.E., Ricker, J., Arenth, P., and Berga, S.L. (2012). Persistent hypogonadism influences estradiol synthesis, cognition, and outcome in males after severe TBI. Brain Inj. 26, 1226-1242.
14. Sowers, M.R., Wilson, A.L., Kardia, S.R., Chu, J., and Ferrell, R. (2006). Aromatase gene (CYP 19) polymorphisms and endogenous androgen concentrations in a multiracial/multiethnic, multisite study of women at midlife. Am. J. Med. 119, 9 Suppl. 1, S23-S30. (Pubitemid 44292099)
15. Bullock, M.R., and Povlishock, J.T. (2007). Guidelines for the management of severe traumatic brain injury. J. Neurotrauma 24, Suppl. 1, S1-S106.
16. Zafonte, R., Friedewald, W.T., Lee, S.M., Levin, B., Diaz-Arrastia, R., Ansel, B.,Eisenberg,H., Timmons, S.D.,Temkin,N.,Novack, T.,Ricker, J.,Merchant, R., and Jallo, J. (2009). The citicoline brain injury treatment (COBRIT) trial: design and methods. J. Neurotrauma 26, 2207-2216.
17. Jennett, B. and Band, M. (1975). Assessment of outcome after severe brain damage. Lancet 1, 480-484.
18. Miller, S.A., Dykes, D.D., and Polesky, H.F. (1988). A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res. 16, 1215.
19. Gibson, C.L., Gray, L.J., Murphy, S.P., and Bath, P.M. (2006). Estrogens and experimental ischemic stroke: a systematic review. J. Cereb. Blood Flow Metab. 26, 1103-1113. (Pubitemid 44268172)
20. McCullough, L.D., Blizzard, K., Simpson, E.R., Oz, O.K., and Hurn, P.D. (2003). Aromatase cytochrome P450 and extragonadal estrogen play a role in ischemic neuroprotection. J. Neurosci. 23, 8701-8705. (Pubitemid 37176650)
21. Mendelowitsch, A., Ritz, M.F., Ros, J., Langemann, H., and Gratzl, O. (2001). 17beta-estradiol reduces cortical lesion size in the glutamate excitotoxicity model by enhancing extracellular lactate: a new neuroprotective pathway. Brain Res. 901, 230-236. (Pubitemid 32718826)
22. Yang, S.H., Shi, J., Day, A.L., and Simpkins, J.W. (2000). Estradiol exerts neuroprotective effects when administered after ischemic insult. Stroke 31, 745-749; discussion, 749-750.
23. Hawk, T., Zhang, Y.Q., Rajakumar, G., Day, A.L., and Simpkins, J.W. (1998). Testosterone increases and estradiol decreases middle cerebral artery occlusion lesion size in male rats. Brain Res. 796, 296-298. (Pubitemid 28343260)
24. Cheng, J., Alkayed, N.J., and Hurn, P.D. (2007). Deleterious effects of dihydrotestosterone on cerebral ischemic injury. J. Cereb. Blood Flow Metab. 27, 1553-1562. (Pubitemid 47301443)
25. Yang, S.H., Perez, E., Cutright, J., Liu, R., He, Z., Day, A.L., and Simpkins, J.W. (2002). Testosterone increases neurotoxicity of glutamate in vitro and ischemia-reperfusion injury in an animal model. J. Appl. Physiol. 92, 195-201. (Pubitemid 34670006)
26. Beaumont, A., Marmarou, A., Hayasaki, K., Barzo, P., Fatouros, P., Corwin, F., Marmarou, C., and Dunbar, J. (2000). The permissive nature of blood brain barrier (BBB) opening in edema formation following traumatic brain injury. Acta. Neurochir. Suppl. 76, 125-129.
27. Eriksson, A.L., Lorentzon, M., Vandenput, L., Labrie, F., Lindersson, M., Syvanen, A.C., Orwoll, E.S., Cummings, S.R., Zmuda, J.M., Ljunggren, O., Karlsson, M.K., Mellstrom, D., and Ohlsson, C. (2009). Genetic variations in sex steroid-related genes as predictors of serum estrogen levels in men. J. Clin. Endocrinol. Metab. 94, 1033-1041.
28. Hobbs, C.J., Jones, R.E., and Plymate, S.R. (1992). The effects of sex hormone binding globulin (SHBG) on testosterone transport into the cerebrospinal fluid. J. Steroid Biochem. Mol. Biol. 42, 629-635.
29. Savaridas, T., Andrews, P.J., and Harris, B. (2004). Cortisol dynamics following acute severe brain injury. Intensive Care Med. 30, 1479-1483. (Pubitemid 38951735)
30. Dossett, L.A., Swenson, B.R., Heffernan, D., Bonatti, H., Metzger, R., Sawyer, R.G., and May, A.K. (2008). High levels of endogenous estrogens are associated with death in the critically injured adult. J. Trauma 64, 580-585. (Pubitemid 351366872)
31. May, A.K., Dossett, L.A., Norris, P.R., Hansen, E.N., Dorsett, R.C., Popovsky, K.A., and Sawyer, R.G. (2008). Estradiol is associated with mortality in critically ill trauma and surgical patients. Crit. Care Med. 36, 62-68.
32. Spratt, D.I., Morton, J.R., Kramer, R.S., Mayo, S.W., Longcope, C., and Vary, C.P. (2006). Increases in serum estrogen levels during major illness are caused by increased peripheral aromatization. Am. J. Physiol. Endocrinol. Metab. 291, E631-E638. (Pubitemid 44352271)
33. Zwain, I.H., and Yen, S.S. (1999). Neurosteroidogenesis in astrocytes, oligodendrocytes, and neurons of cerebral cortex of rat brain. Endocrinology 140, 3843-3852. (Pubitemid 30645442)
34. Balthazart, J., Baillien, M., and Ball, G.F. (2006). Rapid control of brain aromatase activity by glutamatergic inputs. Endocrinology 147, 359-366. (Pubitemid 43004289)
35. Jiang, J., Tang, N.L., Ohlsson, C., Eriksson, A.L., Vandenput, L., Chan, F.W., Ching, J.K., Kwok, A., Orwoll, E., Kwok, T.C., Woo, J., and Leung, P.C. (2010). Association of genetic variations in aromatase gene with serum estrogen and estrogen/testosterone ratio in Chinese elderly men. Clin. Chim. Acta 411, 53-58.
36. Koudu, Y., Onouchi, T., Hosoi, T., and Horiuchi, T. (2012). Association of CYP19 gene polymorphism with vertebral fractures in japanese postmenopausal women. Biochem. Genet. 50, 389-396.
37. Sofi, M., Young, M.J., Papamakarios, T., Simpson, E.R., and Clyne, C.D. (2003). Role of CRE-binding protein (CREB) in aromatase expression in breast adipose. Breast Cancer Res. Treat. 79, 399-407. (Pubitemid 36750947)
38. Pennypacker, K.R., Kassed, C.A., Eidizadeh, S., and O'Callaghan, J.P. (2000). Brain injury: prolonged induction of transcription factors. Acta Neurobiol. Exp. (Wars) 60, 515-530.
39. Guo, Y., Xiong, D.H., Yang, T.L., Guo, Y.F., Recker, R.R., and Deng, H.W. (2006). Polymorphisms of estrogen-biosynthesis genes CYP17 and CYP19 may influence age at menarche: a genetic association study in Caucasian females. Hum. Mol. Genet. 15, 2401-2408. (Pubitemid 44288694)
40. Garcia-Casado, Z., Guerrero-Zotano, A., Llombart-Cussac, A., Calatrava, A., Fernandez-Serra, A., Ruiz-Simon, A., Gavila, J., Climent, M.A., Almenar, S., Cervera-Deval, J., Campos, J., Albaladejo, C.V., Llombart-Bosch, A., Guillem, V., and Lopez-Guerrero, J.A. (2010). A polymorphism at the 3¢-UTR region of the aromatase gene defines a subgroup of postmenopausal breast cancer patients with poor response to neoadjuvantletrozole. BMC Cancer 10, 36.
41. Xu, W.H., Dai, Q., Xiang, Y.B., Long, J.R., Ruan, Z.X., Cheng, J.R., Zheng, W., and Shu, X.O. (2007). Interaction of soy food and tea consumption with CYP19A1 genetic polymorphisms in the development of endometrial cancer. Am. J. Epidemiol. 166, 1420-1430. (Pubitemid 350209050)
42. Haiman, C.A., Dossus, L., Setiawan, V.W., Stram, D.O., Dunning, A.M., Thomas, G., Thun, M.J., Albanes, D., Altshuler, D., Ardanaz, E., Boeing, H., Buring, J., Burtt, N., Calle, E.E., Chanock, S., Clavel-Chapelon, F., Colditz, GA., Cox, D.G., Feigelson, H.S., Hankinson, S.E., Hayes, R.B., Henderson, B.E., Hirschhorn, J.N., Hoover, R., Hunter, D.J., Kaaks, R., Kolonel, L.N., Le Marchand, L., Lenner, P., Lund, E., Panico, S., Peeters, P.H., Pike, M.C., Riboli, E., Tjonneland, A., Travis, R., Trichopoulos, D., Wacholder, S., and Ziegler, R.G. (2007). Genetic variation at the CYP19A1 locus predicts circulating estrogen levels but not breast cancer risk in postmenopausal women. Cancer Res. 67, 1893-1897. (Pubitemid 46424203)
43. Colomer, R., Monzo, M., Tusquets, I., Rifa, J., Baena, J.M., Barnadas, A., Calvo, L., Carabantes, F., Crespo, C., Munoz, M., Llombart, A., Plazaola, A., Artells, R., Gilabert, M., Lloveras, B., and Alba, E. (2008). A single-nucleotide polymorphism in the aromatase gene is associated with the efficacy of the aromatase inhibitor letrozole in advanced breast carcinoma. Clin. Cancer Res. 14, 811-816. (Pubitemid 351231164)
44. Farace, E., and Alves, W.M. (2000). Do women fare worse: a metaanalysis of gender differences in traumatic brain injury outcome. J. Neurosurg. 93, 539-545. (Pubitemid 32799285)
45. Farin, A., Deutsch, R., Biegon, A., and Marshall, L.F. (2003). Sexrelated differences in patients with severe head injury: greater susceptibility to brain swelling in female patients 50 years of age and younger. J. Neurosurg. 98, 32-36. (Pubitemid 36050444)
46. Wagner, A.K., Hammond, F.M., Sasser, H.C., Wiercisiewski, D., and Norton, H.J. (2000). Use of injury severity variables in determining disability and community integration after traumatic brain injury. J. Trauma 49, 411-419.
47. Clifton, G.L., Valadka, A., Zygun, D., Coffey, C.S., Drever, P., Fourwinds, S., Janis, L.S., Wilde, E., Taylor, P., Harshman, K., Conley, A., Puccio, A., Levin, H.S., McCauley, S.R., Bucholz, R.D., Smith, K.R., Schmidt, J.H., Scott, J.N., Yonas, H., and Okonkwo, D.O. (2011). Very early hypothermia induction in patients with severe brain injury (the National Acute Brain Injury Study: Hypothermia II): a randomised trial. Lancet Neurol. 10, 131-139.
48. Wright, D.W., Kellermann, A.L., Hertzberg, V.S., Clark, P.L., Frankel, M., Goldstein, F.C., Salomone, J.P., Dent, L.L., Harris, O.A., Ander, D.S., Lowery, D.W., Patel, M.M., Denson, D.D., Gordon, A.B., Wald, M.M., Gupta, S., Hoffman, S.W., and Stein, D.G. (2007). ProTECT: a randomized clinical trial of progesterone for acute traumatic brain injury. Ann. Emerg. Med. 49, 391-402, 402.e1-2.