Sex of the cell dictates its response: Differential gene expression and sensitivity to cell death inducing stress in male and female cells

FASEB Journal

Volumn 23, Issue 6, 2009, Pages 1869-1879

  Penaloza, Carlos ^a   Estevez, Brian ^a   Orlanski, Shari ^a   Sikorska, Marianna ^b   Walker, Roy ^b   Smith, Catherine ^b   Smith, Brandon ^b   Lockshin, Richard A ^c   Zakeri, Zahra ^a  

^a CITY UNIVERSITY OF NEW YORK   (United States)

^b NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^c ST JOHN'S UNIVERSITY   (United States)

Author keywords

Apoptosis; Estrogen; Ethanol; Gender; Testosterone

Indexed keywords

ALCOHOL; CAMPTOTHECIN; SEX HORMONE; ESTROGEN; TESTOSTERONE;

ADOLESCENT; ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL CULTURE; CELL ISOLATION; CELL STRESS; CELL VIABILITY; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEX; SEX DIFFERENTIATION; ANIMAL; ANIMAL EMBRYO; CELL DEATH; CYTOLOGY; DNA FRAGMENTATION; GENDER AND SEX; MALE; METABOLISM; MICROARRAY ANALYSIS; MOLECULAR GENETICS; PHYSIOLOGY; PREGNANCY; SEXUAL DEVELOPMENT;

INFLUENZA A VIRUS; MUS;

ANIMALS; CELL DEATH; CELLS, CULTURED; DNA FRAGMENTATION; EMBRYO, MAMMALIAN; ESTROGENS; ETHANOL; FEMALE; GENE EXPRESSION; MALE; MICE; MICROARRAY ANALYSIS; MOLECULAR SEQUENCE DATA; PREGNANCY; SEX CHARACTERISTICS; SEX DETERMINATION (GENETICS); TESTOSTERONE;

EID: 67649380838     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.08-119388     Document Type: Article

References (32)

1. Ceribelli, A., Pino, M. S., and Cecere, F. L. (2007) Gender differences: implications for clinical trials and practice. J. Thorac. Oncol. 2, 15-18
2. Bain, C. F. D., Speizer, F. E., Thun, M., Hertzmark, E., Rosner, B. A., and Colditz, G. A. (2004) Lung cancer rates in men and women with comparable histories of smoking. J. Natl. Cancer Inst. 96, 826-834
3. Beeson, P. (1994) Age and sex association of 40 autoimmune diseases. Am. J. Med. 96, 457-462
4. 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
5. Lockshin, M. D. (2001) Invited review: sex ratio and rheumatic disease. J. Appl. Physiol. 91, 2366-2373
6. Lockshin, M. D. (2006) Sex differences in autoimmune disease. Orthop. Clin. North Am. 37, 629-633
7. Shulman, L. M., and Bhat, V. (2006) Gender disparities in Parkinson's disease. Expert Rev. Neurother. 6, 407-416
8. Vaccarino, V., Parsons, L., Every, N. R., Barron, H. V., and Krumholz, H. M. (1999) Sex-based differences in early mortality after myocardial infarction. N. Engl. J. Med. 341, 217-225
9. Zorgdrager, A., and Keyser, J. D. (2002) The premenstrual period and exacerbations in multiple sclerosis. Eur. Neurol. 48, 204-206
10. Gompel, A., and Piette, J. C. (2007) Systemic lupus erythematosus and hormone replacement therapy. Menopause Int. 13, 65-70
11. Lockshin, M. D., and Buyon, J. P. (2007) Estrogens and lupus: Bubbling cauldron or another overrated witches' brew? Arthritis Rheum. 56, 1048-1050
12. Du, L., Bayir, H., Lai, Y., Zhang, X., Kochanek, P. M., Watkins, S. C., Graham, S. H., and Clark, R. S. B. (2004) Innate gender-based proclivity in response to cytotoxicity and programmed cell death pathway. J. Biol. Chem. 279, 38563-38570
13. Heyer, A., Hasselblatt, M., von Ahsen, N., Hafner, H., Siren, A.-L., and Ehrenreich, H. (2005) In vitro gender differences in neuronal survival on hypoxia and in 17β-estradiol-mediated neuroprotection. J. Cereb. Blood Flow Metab. 25, 427-430
14. Nikezic-Ardolic, M., Lin, L., Milcevic, M., and Zakeri, Z. (1999) Gender differences in cellular response. Lupus 8, 375-379
15. Amador-Noguez, D., Zimmerman, J., Venable, S., and Darlington, G. (2005) Gender-specific alterations in gene expression and loss of liver sexual dimorphism in the long-lived Ames dwarf mice. Biochem. Biophys. Res. Commun. 332, 1086-1100
16. Dewing, P., Shi, T., Horvath, S., and Vilain, E. (2003) Sexually dimorphic gene expression in mouse brain precedes gonadal differentiation. Mol. Brain Res. 118, 82-90
17. Xu, J., Burgoyne, P. S., and Arnold, A. P. (2002) Sex differences in sex chromosome gene expression in mouse brain. Hum. Mol. Genet. 11, 1409-1419
18. Dulos, J., van der Vleuten, M. A., Kavelaars, A., Heijnen, C. J., and Boots, A. M. (2005) CYP7B expression and activity in fibroblast-like synoviocytes from patients with rheumatoid arthritis: regulation by proinflammatory cytokines. Arthritis Rheum. 52, 770-778 (Pubitemid 40365098)
19. Higashi, E., Fukami, T., Itoh, M., Kyo, S., Inoue, M., Yokoi, T., and Nakajima, M. (2007) Human CYP2A6 is induced by estrogen via estrogen receptor. Drug Metab. Dispos. 35, 1935-1941
20. Isensee, J., Witt, H., Pregla, R., Hetzer, R., Regitz-Zagrosek, V., and Ruiz Noppinger, P. (2008) Sexually dimorphic gene expression in the heart of mice and men. J. Molec. Med. 86, 61-74
21. Mollerup, S., Ryberg, D., Hewer, A., Phillips, D. H., and Haugen, A. (1999) Sex differences in lung CYP1A1 expression and DNA adduct levels among lung cancer patients. Cancer Res. 59, 3317-3320 (Pubitemid 29334483)
22. Nickerson, M., Kennedy, S. L., Johnson, J. D., and Fleshner, M. (2006) Sexual dimorphism of the intracellular heat shock protein 72 response. J. Appl. Physiol. 101, 566-575
23. Angele, M. K., Nitsch, S., Knoferl, M. W., Ayala, A., Angele, P., Schildberg, F. W., Jauch, K. W., and Chaudry, I. H. (2003) Sex-specific p38 MAP kinase activation following trauma-hemorrhage: involvement of testosterone and estradiol. Am. J. Physiol. Endocrinol. Metab. 285, E189-196
24. Karasavvas, N. E. R., Bittman, R., Lockshin, R., Hockenbery, D., and Zakeri, Z. (1996) BCL-2 suppresses ceramide-induced cell killing. Cell Death Differ. 3, 149-151
25. Ahuja, H. S., James, W., and Zakeri, Z. (1997) Rescue of the limb deformity in Hammertoe mutant mice by retinoic acid-induced cell death. Dev. Dyn. 208, 466-481
26. Colantuoni, C., Henry, G., Zeger, S., and Pevsner, J. (2002) SNOMAD (standardization and normalization of microarray data): web-accessible gene expression data analysis. Bioinformatics 18, 1540-1541 (Pubitemid 35414548)
27. Workman, C., Jensen, L. J., Jarmer, H., Berka, R., Gautier, L., Nielser, H. B., Saxild, H.-H., Nielsen, C., Brunak, S., and Knudsen, S. (2002) A new non-linear normalization method for reducing variability in DNA microarray experiments. Genome Biol. 3, 1-16
28. Diehn, M., Sherlock, G., Binkley, G., Jin, H., Matese, J. C., Hernandez-Boussard, T., Rees, C. A., Cherry, J. M., Botstein, D., Brown, P. O., and Alizadeh, A. A. (2003) SOURCE: a unified genomic resource of functional annotations, ontologies, and gene expression data. Nucleic Acids Res. 31, 219-223 (Pubitemid 36150369)
29. Walker, R., Smith, B., Liu, Q. Y., Fazel, F., Valdes, J. J., Liu, Z., and Lach, B. (2004) Data mining of gene expression changes in Alzheimer brain. Artif. Intell. Med. 31, 137-154
30. Peippo, J., Farazmand, A., Kurkilahti, M., Markkula, M., Basrur, P. K., and King, W. A. (2002) Sex-chromosome linked gene expression in in-vitro produced bovine embryos. Mol. Hum. Reprod. 8, 923-929
31. Rose, K. A., Stapleton, G., Dott, K., Kieny, M. P., Best, R., Schwarz, M., Russell, D. W., Björkhem, L., Seckl, J., and Lathe, R. (1997) Cyp7b, a novel brain cytochrome P450, catalyzes the synthesis of neurosteroids 7a-hydroxy dehydroepiandrosterone and 7a-hydroxy pregnenolone. Proc. Natl. Acad. Sci. USA 94, 4925-4930
32. Tang, W., and Norlin, M. (2006) Regulation of steroid hydroxylase CYP7B1 by androgens and estrogens in prostate cancer LNCaP cells. Biochem. Biophys. Res. Commun. 344, 540-546