Molecular Biology Reports

, Volume 45, Issue 6, pp 2571–2584 | Cite as

Oxidant stress induction and signalling in xenografted (human breast cancer-tissues) plus estradiol treated or N-ethyl-N-nitrosourea treated female rats via altered estrogen sulfotransferase (rSULT1E1) expressions and SOD1/catalase regulations

  • Aarifa Nazmeen
  • Smarajit MaitiEmail author
Original Article


N-ethyl-N-nitrosourea (ENU) is highly used in rodent models of tumerogenesis/carcinogenesis. Xenografting human-cancer tissues/cells with estradiol (E2) treatment is also used to generate rodent-models of gynaecological cancers. The altered metabolic-redox environment leading to establishment of pre-tumorigenesis condition and their mechanism are less studied. Here, female Wister rats were treated with these drugs at their pre-tumerogenic dosage (one group ENU single intra-peritoneal dose of 90 mg/kg b.w. and another group were implanted with human breast tumor (stage-IIIB) and fed with 2.5 mg of 17β-estradiol once in a week for 4 months). After 4 months, animals were sacrificed; their serum and liver tissues were tested. A brief comparison was made with a rat model (regarded as positive control) of toxicity induced by mutagenic environmental pollutant arsenic (0.6 ppm daily/4 weeks). The increase in serum alkaline phosphatase and glutamate-pyruvate transaminase suggests the possible organ toxicity is favoured by the increase in hepatic/systemic free radicals and oxidative stress in all drug application models. But the increase in the serum E2 level as noted in the ELISA data with impairment in the hepatic estrogen sulfotransferase (SULT1E1) protein expression (immuno-blot data) were noticed with interfered hepatic free-thiols only in ENU and xenograft-E2 group compared to arsenic group. It is also evident in the in vitro result from E2/GSH/NAC added hepatic slices with altered antioxidant regulations. Moreover, impairment in hepatic SOD1, catalase and glutathiole peroxidase activities (PAGEzymographic data), especially in the ENU-treated group makes them more vulnerable to the oxidative threat in creating pre-tumerogenic microenvironment. This is evident in the result of their higher DNA-damage and histological abnormalities. The Bioinformatics study revealed an important role of rSULT1E1 in the regulations of E2 metabolism. This study is important for the exploration of the pre-tumerogenic condition by ENU and E2 by impairing SULT1E1 expression and E2 regulations via oxidant-stress signalling. The finding may help to find new therapeutic-targets to treat gynaecological-cancers more effectively.


N-ethyl-N-nitrosourea (ENU) Xenograft-estradiol Hepatocellular toxicity Oxidative stress Estrogen sulfotransferase 



University Grants Commission, New Delhi provided JRF and SRF to AN who is a Ph.D. students working in the Post Graduate Department of Biochemistry, OIST.

Compliance with ethical standards

Conflicting interest

The author(s) declared no potential conflicts of interests with respect to the authorship and/or publication of this article.


  1. 1.
    Dietrich CG, Rau M, Jahn D, Geier A (2017) Changes in drug transport and metabolism and their clinical implications in non-alcoholic fatty liver disease. Expert Opin Drug MetabToxicol 13(6):625–640CrossRefGoogle Scholar
  2. 2.
    Tsubura A, Lai YC, Miki H, Sasaki T, Uehara N, Yuri T, Yoshizawa K (2011) Animal models of N-methyl-N-nitrosourea-induced mammary cancer and retinal degeneration with special emphasis on therapeutic trials. In Vivo 25(1):11–22PubMedGoogle Scholar
  3. 3.
    Gurley KE, Moser RD, Kemp CJ (2015) Induction of liver tumors in mice with N-ethyl-N-nitrosourea or N-nitrosodiethylamine. Cold Spring Harb Protoc 2015(10):941–942CrossRefGoogle Scholar
  4. 4.
    Stottmann R, Beier D (2014) ENU mutagenesis in the mouse. Curr Protoc Mouse Biol 4(2):25–35CrossRefGoogle Scholar
  5. 5.
    Coghill EL, Hugill A, Parkinson N, Davison C, Glenister P, Clements S, Hunter J, Cox RD, Brown SD (2002) A gene-driven approach to the identification of ENU mutants in the mouse. Nat Genet 30(3):255–256CrossRefGoogle Scholar
  6. 6.
    Barbaric IWS, Russ A. Dear TN (2007) Spectrum of ENU-induced mutations in phenotype-driven and gene-driven screens in the mouse. Environ Mol Mutagen 48:124–142CrossRefGoogle Scholar
  7. 7.
    Shrivastav N, Li D, Essigmann JM (2010) Chemical biology of mutagenesis and DNA repair: cellular responses to DNA alkylation. Carcinogenesis 31:59–70CrossRefGoogle Scholar
  8. 8.
    Engelbergs J, Thomale J, Rajewsky MF (2000) Role of DNA repair in carcinogen-induced ras mutation. Mutat Res 450:139–153CrossRefGoogle Scholar
  9. 9.
    Thordarson G, Lee AV, McCarty M, Van Horn K, Chu O, Chou YC, Yang J, Guzman RC, Nandi S, Talamantes F (2001) Growth and characterization of N-methyl-N-nitrosourea-induced mammary tumors in intact and ovariectomized rats. Carcinogenesis 22(12):2039–2047CrossRefGoogle Scholar
  10. 10.
    Katayama K, Ueno M, Takai H, Ejiri N, Uetsuka K, Nakayama H, Doi K (2002) Ethylnitrosourea induces apoptosis and growth arrest in the trophoblastic cells of rat placenta. Biol Reprod 67(2):431–435CrossRefGoogle Scholar
  11. 11.
    Liou GY, Storz P (2010) Reactive oxygen species in cancer. Free Radic Res 44(5):479–496CrossRefGoogle Scholar
  12. 12.
    Sanchez-Perez Y, Carrasco-Legleu C, Garcia-Cuellar C, Pérez-Carreon J, Hernández-Garcia S, Salcido-Neyoy M, Aleman-Lazarini L, Villa-Trevino S (2005) Oxidative stress in carcinogenesis. Correlation between lipid peroxidation and induction of preneoplastic lesions in rat hepatocarcinogenesis. Cancer Lett 217(1):25–32CrossRefGoogle Scholar
  13. 13.
    Yager JD, Davidson N (2006) Estrogen carcinogenesis in breast cancer. Engl J Med 354:270–282CrossRefGoogle Scholar
  14. 14.
    Deblois G, Giguère V (2011) Functional and physiological genomics of estrogen-related receptors (ERRs) in health and disease. Biochim Biophys Acta 1812(8):1032–1040CrossRefGoogle Scholar
  15. 15.
    Russo J, Russo IH (2006) The role of estrogen in the initiation of breast cancer. J Steroid Biochem Mol Biol 102:89–96CrossRefGoogle Scholar
  16. 16.
    Boukari K, Ciampi ML, Guiochon MA, Young J, Lombes M, Meduri G (2007) Human fetal testis: source of estrogen and target of estrogen action. Hum Reprod 7:1885–1892CrossRefGoogle Scholar
  17. 17.
    Beckman KB, Ames BN (1998) The free radical theory of aging matures. Physiol Rev 78(2):547–581CrossRefGoogle Scholar
  18. 18.
    Nelson HD, Zakher B, Cantor A, Fu R, Griffin JO, Meara ES, Buist DS, Kerlikowske K, van Ravesteyn NT, Trentham-Dietz A, Mandelblatt JS, Miglioretti DL (2012) Risk factors for breast cancer for women aged 40 to 49 years: a systematic review and meta-analysis. Ann Intern Med 156(9), 635–648CrossRefGoogle Scholar
  19. 19.
    Benz CC, Yau C (2008) Ageing, oxidative stress and cancer: paradigms in parallax. Nat Rev Cancer 8(11):875–879CrossRefGoogle Scholar
  20. 20.
    Maria BR, Elaine R, Nancy D, Maureen KW, Charles EW (2012) Genomics of estradiol-3-sulfate action in the ovine fetal hypothalamus. Physiol Genom 44(13):669–677CrossRefGoogle Scholar
  21. 21.
    Maiti S, Zhang J, Chen G (2007) Redox regulation of human estrogen sulfotransferase (hSULT1E1). Biochem Pharmacol 73(9):1474–1481CrossRefGoogle Scholar
  22. 22.
    Pasqualini JR, Chetrite GS (2007) Correlation of estrogen sulfotransferase activity and proliferation in normal and carcinomatous human breast. A hypothesis. Anticancer Res 27(5A):3219–3225PubMedGoogle Scholar
  23. 23.
    Santarelli RL, Pierre F, Corpet DE (2008) Processed meat and colorectal cancer: a review of epidemiologic and experimental evidence. Nutr Cancer 60(2):131–144CrossRefGoogle Scholar
  24. 24.
    Maiti S, Chattopadhyay S, Deb B, Samanta T, Maji G, Pan B, Ghosh A, Ghosh D (2012) Antioxidant and metabolic impairment result in DNA damage in arsenic-exposed individuals with severe dermatological manifestations in Eastern India. Environ Toxicol 27(6):342–350CrossRefGoogle Scholar
  25. 25.
    Wu YJ, Muldoon LL, Dickey DT, Lewin SJ, Varallyay CG, Neuwelt EA (2009) Cyclophosphamide enhances human tumor growth in nude rat xenografted tumor Models. Neoplasia 11(2):187–195CrossRefGoogle Scholar
  26. 26.
    Ligresti A, Moriello AS, Starowicz K, Matias I, Pisanti S, De Petrocellis L, Laezza C, Portella G, Bifulco M, Di Marzo V (2006) Antitumor activity of plant cannabinoids with emphasis on the effect of cannabidiol on human breast carcinoma. J Pharmacol Exp Ther 318(3):1375–1387CrossRefGoogle Scholar
  27. 27.
    Gordon MN, Osterburg HH, May PC, Finch CE (1986) Effective oral administration of 17 beta-estradiol to female C57BL/6J mice through the drinking water. Biol Rep 35(5):1088–1095CrossRefGoogle Scholar
  28. 28.
    Levin-Allerhand JA, Sokol K, Smith JD (2003) Safe and effective method for chronic 17beta-estradiol administration to mice. Contemp Top Lab Anim Sci 42(6):33–35PubMedGoogle Scholar
  29. 29.
    Mense SM, Remotti F, Bhan A, Singh B, El-Tamer M, Hei TK, Bhat HK (2008) Estrogen-induced breast cancer: alterations in breast morphology and oxidative stress as a function of estrogen exposure. Toxicol Appl Pharmacol 232:78–85CrossRefGoogle Scholar
  30. 30.
    Stoica G, Koestner A, Capen CC (1984) Neoplasms induced with high single doses of N-ethyl-N-nitrosourea in 30-day-old Sprague-Dawley rats, with special emphasis on mammary neoplasia. Anticancer Res 4(1–2):5–12PubMedGoogle Scholar
  31. 31.
    Pacheco-Martínez MM, Cortés-Barberena E, Cervantes-Ríos E, Del Carmen García-Rodríguez M, Rodríguez-Cruz L, Ortiz-Muñiz R (2016) Moderate malnutrition in rats induces somatic gene mutations. Mutat Res 789:26–32CrossRefGoogle Scholar
  32. 32.
    Zaizen Y, Higuchi Y, Matsuo N, Shirabe K, Tokuda H, Takeshita M (2000) Antitumor effects of soybean hypocotyls and soybeans on the mammary tumor induction by N-methyl-n-nitrosourea in F344 rats. Anticancer Res 20(3A):1439–1444PubMedGoogle Scholar
  33. 33.
    Acharyya N, Sajed Ali S, Deb B, Chattopadhyay S, Maiti S (2015) Green tea (Camellia sinensis) alleviates arsenic-induced damages to DNA and intestinal tissues in rat and in situ intestinal loop by reinforcing antioxidant system. Environ Toxicol 30(9):1033–1044CrossRefGoogle Scholar
  34. 34.
    Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275PubMedPubMedCentralGoogle Scholar
  35. 35.
    Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302–310CrossRefGoogle Scholar
  36. 36.
    Forman HJ (2009) Critical methods in free radical biology & medicine. Free Radic Biol Med 47:S207CrossRefGoogle Scholar
  37. 37.
    Gamero-Sandemetrio E, Gómez-Pastor R, Matallana E (2017) Zymography methods to simultaneously analyze superoxide dismutase and catalase activities: novel application for yeast species identification. Methods Mol Biol 1626:189–198CrossRefGoogle Scholar
  38. 38.
    Christine JW, Joseph JC (2010) Measurement of superoxide dismutase, catalase, and glutathione peroxidase in cultured cells and tissue. Nat Protoc 5(1):51–66CrossRefGoogle Scholar
  39. 39.
    Acharyya N, Chattopadhyay S, Maiti S (2014) Chemoprevention against arsenic-induced mutagenic DNA breakage and apoptotic liver damage in rat via antioxidant and SOD1 upregulation by green tea (Camellia sinensis) which recovers broken DNA resulted from arsenic-H2O2 related in vitro oxidant stress. J Environ Sci Health C 32(4):338–361CrossRefGoogle Scholar
  40. 40.
    Jensen LJ, Kuhn M, Stark M, Chaffron S, Creevey C, Muller J, Doerks T, Julien P, Roth A, Simonovi M, Bork P, von Mering C (2009) STRING 8—a global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res 37:412–416CrossRefGoogle Scholar
  41. 41.
    Taboada B, Verde C, Merino E (2010) High accuracy operon prediction method based on STRING database scores. Nucleic Acids Res 38:130CrossRefGoogle Scholar
  42. 42.
    Von Mering C, Jensen LJ, Snel B, Hooper SD, Krupp M, Foglierini M, Jouffre N, Huynen MA, Bork P (2005) STRING: known and predicted protein-protein associations, integrated and transferred across organisms. Nucleic Acids Res 33:D433–D437CrossRefGoogle Scholar
  43. 43.
    Roomi MW, Roomi NW, Ivanov V, Kalinovsky T, Niedzwiecki A, Rath M (2005) Modulation of N-methyl-N-nitrosourea induced mammary tumors in Sprague-Dawley rats by combination of lysine, proline, arginine, ascorbic acid and green tea extract. Breast Cancer Res 7(3):R291–R295CrossRefGoogle Scholar
  44. 44.
    Morton CL, Houghton PJ (2007) Establishment of human tumor xenografts in immunodeficient mice. Nat Protoc 2(2):247–250CrossRefGoogle Scholar
  45. 45.
    Morton JJ, Bird G, Refaeli Y, Jimeno A (2016) Humanized mouse xenograft models: narrowing the tumor-microenvironment gap. Cancer Res 76(21):6153–6158CrossRefGoogle Scholar
  46. 46.
    Yesennia SP, Claudia CL, Claudia GC, Julio PC, Sergio HG, Martha SN, Leticia AL, Saul VT (2005) Correlation between lipid peroxidation and induction of preneoplastic lesions in rat hepatocarcinogenesis. Oxidative stress in carcinogenesis. Cancer Lett 217(1):25–32CrossRefGoogle Scholar
  47. 47.
    Lander HM (1997) An essential role for free radicals and derived species in signal transduction. FASEB J 11:118–124CrossRefGoogle Scholar
  48. 48.
    Felty Q, Singh KP, Roy D (2005) Estrogen-induced G1/S transition of G0-arrested estrogen-dependent breast cancer cells is regulated by mitochondrial oxidant signaling. Oncogene 24:4883–4893CrossRefGoogle Scholar
  49. 49.
    Qiu Y, Waters CE, Lewis AE, Langman MJ, Eggo MC (2002) Oestrogen-induced apoptosis in colonocytes expressing oestrogen receptor beta. J Endocrinol 174(3):369–377CrossRefGoogle Scholar
  50. 50.
    Luan Y, Qi X, Xu L, Ren J, Chen T (2014) Absence of mature microRNAs inactivates the response of gene expression to carcinogenesis induced by N-ethyl-N-nitrosourea in mouse liver. J Appl Toxicol 34(12):1409–1417CrossRefGoogle Scholar
  51. 51.
    Jardim BV, Moschetta MG, Leonel C, Gelaleti GB, Regiani VR, Ferreira LC, Lopes JR, Zuccari DA (2013) Glutathione and glutathione peroxidase expression in breast cancer: an immunohistochemical and molecular study. Oncol Rep 30(3):1119–1128CrossRefGoogle Scholar
  52. 52.
    Liu J, Hinkhouse MM, Sun W, Weydert CJ, Ritchie JM, Oberley LW, Cullen JJ (2004) Redox regulation of pancreatic cancer cell growth: role of glutathione peroxidase in the suppression of the malignant phenotype. Hum Gene Ther 15(3):239–250CrossRefGoogle Scholar
  53. 53.
    Kilic N, Yavuz Taslipinar M, Guney Y, Tekin E, Onuk E (2014) An investigation into the serum thioredoxin, superoxide dismutase, malondialdehyde, and advanced oxidation protein products in patients with breast cancer. Ann Surg Oncol 21(13):4139–4143CrossRefGoogle Scholar
  54. 54.
    Silig Y, Ozdemir O, Atalay A (2003) Liver and colon pro- and anti-oxidant enzyme activities in rats after long-term ethylnitrosourea exposure. Indian J Biochem Biophys 40(2):136–138PubMedGoogle Scholar
  55. 55.
    Chattopadhyay S, Deb B, Maiti S (2012) Hepatoprotective role of vitamin B(12) and folic acid in arsenic intoxicated rats. Drug Chem Toxicol 35(1):81–88CrossRefGoogle Scholar
  56. 56.
    Stark AA, Russell JJ, Langenbach R, Pagano DA, Zeiger E, Huberman E (1994) Localization of oxidative damage by a glutathione-gamma-glutamyltranspeptidase system in preneoplastic lesions in sections of livers from carcinogen-treated rats. Carcinogenesis 15(2):343–348CrossRefGoogle Scholar
  57. 57.
    Zhang H, Forman HJ, Choi J (2005) Gamma glutamyl transpeptidase in glutathione biosynthesis. Methods Enzymol 401:468–483CrossRefGoogle Scholar
  58. 58.
    Hanigan MH (2014) Gamma-glutamyl transpeptidase: redox regulation and drug resistance. Adv Cancer Res 122:103–141CrossRefGoogle Scholar
  59. 59.
    Dabrosin C, Ollinger K (2004) Variability of glutathione during the menstrual cycle-due to estrogen effects on hepatocytes? Free Radic Biol Med 36(2):145–151CrossRefGoogle Scholar
  60. 60.
    Calatayud M, Devesa V, Velez D (2013) Differential toxicity and gene expression in Caco-2 cells exposed to arsenic species. Toxicol Lett 218:70–80CrossRefGoogle Scholar
  61. 61.
    Shah MH, Liu GS, Thompson EW, Dusting GJ, Peshavariya HM (2015) Differential effects of superoxide dismutase and superoxide dismutase/catalase mimetics on human breast cancer cells. Breast Cancer Res Treat 150(3):523–534CrossRefGoogle Scholar
  62. 62.
    Li M, Cai JF, Chiu JF (2002) Arsenic induces oxidative stress and activates stress gene expressions in cultured lung epithelial cells. J Cell Biochem 87:29–38CrossRefGoogle Scholar
  63. 63.
    Chattopadhyay S, Maiti S, Maji G, Deb B, Pan B, Ghosh D (2011) Protective role of Moringa oleifera (Sajina) seed on arsenic-induced hepatocellular degeneration in female albino rats. Biol Trace Elem Res 142(2):200–212CrossRefGoogle Scholar
  64. 64.
    Lantz RC, Hays AM (2006) Role of oxidative stress in arsenic-induced toxicity. Drug Metab Rev 38(4):791–804CrossRefGoogle Scholar
  65. 65.
    Unfer TC, Figueiredo CG. Zanchi MM, Maurer LH, Kemerich DM, Duarte MM, Konopka CK, Emanuelli T (2015) Estrogen plus progestin increase superoxide dismutase and total antioxidant capacity in postmenopausal women. Climacteric 18(3):379–388CrossRefGoogle Scholar
  66. 66.
    Guerra RC, Zuniga-Munoz A, Guarner Lans V, Diaz-Diaz E, Tena Betancourt CA, Pérez-Torres I (2014) Modulation of the activities of catalase, Cu-Zn, Mn superoxide dismutase, and glutathione peroxidase in adipocyte from ovariectomised female rats with metabolic syndrome. Int J Endocrinol. CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Singh B, Bhat NK, Bhat HK (2011) Partial inhibition of estrogen-induced mammary carcinogenesis in rats by tamoxifen: balance between oxidant stress and estrogen responsiveness. PLoS ONE 6(9):25125CrossRefGoogle Scholar
  68. 68.
    Liu X, An BH, Kim MJ, Park JH, Kang YS, Chang M (2014) Human glutathione S-transferase P1-1 functions as an estrogen receptor α signaling modulator. Biochem Biophys Res Commun 452(3):840–844CrossRefGoogle Scholar
  69. 69.
    Hachey DL, Dawling S, Roodi N, Parl FF (2003) Sequential action of phase I and II enzymes cytochrome p450 1B1 and glutathione S-transferase P1 in mammary estrogen metabolism. Cancer Res 63(23):8492–8499PubMedGoogle Scholar
  70. 70.
    Mauvais-Jarvis F (2012) Estrogen sulfotransferase: intracrinology meets metabolic diseases. Diabetes 61(6):1353–1354CrossRefGoogle Scholar
  71. 71.
    Sheng-Huang C, Chieh-Hsin C, Mu-Chun Y, Wen-Tung H, Chia-Ying H, Ya-Ting H, Wan-Ling SU. Jiuan-Jen S, Chih-Yang H, Jer-Yuh L (2015) Effects of estrogen on glutathione and catalase levels in human erythrocyte during menstrual cycle. Biomed Rep 3(2):266–268CrossRefGoogle Scholar
  72. 72.
    Guo Y, Hu B, Huang H, Tsung A, Gaikwad NW, Xu M, Jiang M, Ren S, Fan J, Billiar TR, Huang M, Xie W (2015) Estrogen sulfotransferase is an oxidative stress-responsive gene that gender-specifically affects liver ischemia/reperfusion injury. J Biol Chem 290(23):14754–14764CrossRefGoogle Scholar
  73. 73.
    Das Gupta S, So JY, Wall B, Wahler J, Smolarek AK, Sae-Tan S, Soewono KY, Yu H, Lee MJ, Thomas PE, Yang CS, Suh N (2015) Tocopherols inhibit oxidative and nitrosative stress in estrogen-induced early mammary hyperplasia in ACI rats. Mol Carcinog 54(9):916–925CrossRefGoogle Scholar
  74. 74.
    Hu YJ, Diamond AM (2003) Role of glutathione peroxidase 1 in breast cancer: loss of heterozygosity and allelic differences in the response to selenium. Cancer Res 63(12):3347–3351PubMedGoogle Scholar
  75. 75.
    Green PS, Gridley KE, Simpkins JW (1998) Nuclear estrogen receptor-independent neuroprotection by estratrienes: a novel interaction with glutathione. Neuroscience 84(1):7–10CrossRefGoogle Scholar
  76. 76.
    Druwe IL, Sollome JJ, Sanchez-Soria P, Hardwick RN, Camenisch TD, Vaillancourt RR (2012) Arsenite activates NFκB through induction of C-reactive protein. Toxicol Appl Pharmacol 261(3):263–270CrossRefGoogle Scholar
  77. 77.
    Xu Y, Li Y, Li H, Pang Y, Zhao Y, Jiang R, Shen L, Zhou J, Wang X, Liu Q (2013) The accumulations of HIF-1α and HIF-2 α by JNK and ERK are involved in biphasic effects induced by different levels of arsenite in human bronchial epithelial cells. Toxicol Appl Pharmacol 266(2):187–197CrossRefGoogle Scholar
  78. 78.
    Glorieux C, Auquier J, Dejeans N, Sid B, Demoulin JB, Bertrand L, Verrax J, Calderon PB (2014) Catalase expression in MCF-7 breast cancer cells is mainly controlled by PI3K/Akt/mTor signaling pathway. Biochem Pharmacol 89(2):217–223CrossRefGoogle Scholar
  79. 79.
    Manjula RT (2015) Depletion of glutathione during oxidative stress and efficacy of N-acetyl cysteine: an old drug with new approaches. Med Chem 5(1):037–039Google Scholar
  80. 80.
    Sipe HJ Jr, Jordan SJ, Hanna PM, Mason RP (1994) The metabolism of 17 beta-estradiol by lactoperoxidase: a possible source of oxidative stress in breast cancer. Carcinogenesis 15(11):2637–2643CrossRefGoogle Scholar
  81. 81.
    Pullela PK, Alby K, Varela H, Sem DS (2006) Effect of thiol reductants on estrogen and estrogen receptor: revisiting previous assays. FASEB J 20:A74Google Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Department of Biochemistry, Cell & Molecular Therapeutics LabOriental Institute of Science & TechnologyMidnaporeIndia
  2. 2.Department of Biochemistry and Biotechnology, Cell & Molecular Therapeutics LabOriental Institute of Science & TechnologyMidnaporeIndia

Personalised recommendations