Progesterone induces apoptosis of insulin-secreting cells: Insights into the molecular mechanism

Journal of Endocrinology

Volumn 221, Issue 2, 2014, Pages 273-284

  Nunes, V A ^a   Portioli Sanches, E P ^a   Rosim, M P ^a   Araujo, M S ^b   Praxedes Garcia, P ^b   Valle, M M R ^a   Roma, L P ^a   Hahn, C ^c   Gurgul Convey, E ^c   Lenzen, S ^c   Azevedo Martins, A K ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^c HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Apoptosis; Gestational diabetes; Insulin producing cells; Oestriol; Oxidative stress; Progesterone

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ALPHA TOCOPHEROL; BETA TUBULIN; CASPASE 12; CASPASE 3; CASPASE 9; ESTRIOL; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; PROGESTERONE; STAUROSPORINE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CELL MEMBRANE; CELL PROLIFERATION; CELL VIABILITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DNA FRAGMENTATION; ENDOPLASMIC RETICULUM STRESS; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; RAT; RINM5F CELL LINE; WESTERN BLOTTING; ANIMAL; CELL CULTURE; CELL SURVIVAL; CHEMICALLY INDUCED; DRUG EFFECTS; FEMALE; GENETICS; PHYSIOLOGY; PREGNANCY; PREGNANCY DIABETES MELLITUS; SIGNAL TRANSDUCTION; WISTAR RAT;

ANIMALS; APOPTOSIS; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; DIABETES, GESTATIONAL; ESTRIOL; FEMALE; INSULIN-SECRETING CELLS; PREGNANCY; PROGESTERONE; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION;

EID: 84899824238     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-13-0202     Document Type: Article

References (52)

1. Allagnat F, Fukaya S, Nogueira TC, Delaroche D, Welsh N, Marselli L, Marchetti P, Haefliger JA, Eizirik DL&Cardozo AK 2012 C/EBP homologous protein contributes to cytokine-induced pro-inflammatory responses and apoptosis in β-cells. Cell Death and Differentiation 19 1836-1846. (doi:10.1038/cdd.2012.67)
2. Azevedo-Martins AK, Lortz S, Lenzen S, Curi R, Eizirik DL&Tiedge M 2003 Improvement of the mitochondrial antioxidant defense status prevents cytokine-induced nuclear factor-κB activation in insulin-producing cells. Diabetes 52 93-101. (doi:10.2337/diabetes.52.1.93)
3. Bradford MM 1976 A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Analytical Biochemistry 72 248-254. (doi:10.1016/0003-2697(76)90527-3)
4. Butte NF 2000 Carbohydrate and lipid metabolism in pregnancy: normal compared with gestational diabetes mellitus. American Journal of Clinical Nutrition 71 1256S-1261S.
5. Candolfi M, Jaita G, Zaldivar V, Zárate S, Ferrari L, Pisera D, Castro MG & Seilicovich A 2005 Progesterone antagonizes the permissive action of estradiol on tumor necrosis factor-a-induced apoptosis of anterior pituitary cells. Endocrinology 146 736-743. (doi:10.1210/en.2004-1276)
6. Cao SS&Kaufman RJ 2012 Unfolded protein response. Current Biology 22 R622-R626. (doi:10.1016/j.cub.2012.07.004)
7. Cheng X, Shimizu I, Yuan Y, Wei M, Shen M, Huang H, Urata M, Sannomiya K, Fukuno H, Hashimoto Tamaoki T et al. 2006 Effects of estradiol and progesterone on tumor necrosis factor α-induced apoptosis in human hepatoma HuH-7 cells. Life Sciences 79 1988-1994. (doi:10.1016/j.lfs.2006.06.044)
8. Contreras JL, Smyth CA, Bilbao G, Young CJ, Thompson JA&Eckhoff DE 2002 17β-Estradiol protects isolated human pancreatic islets against proinflammatory cytokine-induced cell death: molecular mechanisms and islet functionality. Transplantation 74 1252-1259. (doi:10.1097/00007890-200211150-00010)
9. Dodd JM, Flenady VJ, Cincotta R&Crowther CA 2008 Progesterone for the prevention of preterm birth: a systematic review. Obstetrics and Gynecology 112 127-134. (doi:10.1097/AOG.0b013e31817d0262)
10. Eizirik DL&Cnop M 2010 ER stress in pancreatic β cells: the thin red line between adaptation and failure. Science Signaling 3 pe7. (doi:10.1126/scisignal.3110pe7)
11. Gurgul E, Lortz S, Tiedge M, Jörns A&Lenzen S 2004 Mitochondrial catalase overexpression protects insulin-producing cells against toxicity of reactive oxygen species and proinflammatory cytokines. Diabetes 53 2271-2280. (doi:10.2337/diabetes.53.9.2271)
12. Gyamfi C, Horton AL, Momirova V, Rouse DJ, Caritis SN, Peaceman AM, Sciscione A, Meis PJ, Spong CY, Dombrowski M et al. 2009 The effect of 17-alpha hydroxyprogesterone caproate on the risk of gestational diabetes in singleton or twin pregnancies. American Journal of Obstetrics and Gynecology 201 392.e1-392.e5. (doi:10.1016/j.ajog.2009.06.036)
13. Jabs T 1999 Reactive oxygen intermediates as mediators of programmed cell death in plants and animals. Biochemical Pharmacology 57 231-245. (doi:10.1016/S0006-2952(98)00227-5)
14. Ito Y, Pandey P, Mishra N, Kumar S, Narula N, Kharbanda S, Saxena S & Kufe D 2001 Targeting of the c-Abl tyrosine kinase to mitochondria in endoplasmic reticulum stress-induced apoptosis. Molecular and Cellular Biology 21 6233-6242. (doi:10.1128/MCB.21.18.6233-6242.2001)
15. Jayasooriva GS&Lamont RF 2009 The use of progesterone and other progestational agents to prevent spontaneous preterm labour and preterm birth. Expert Opinion on Pharmacotherapy 10 1007-1016. (doi:10.1517/14656560902851403)
16. Kawai M&Kishi K 1999 Adaptation of pancreatic islet β-cells during the last third of pregnancy: regulation of β-cell function and proliferation by lactogenic hormones in rats. European Journal of Endocrinology 141 419-425. (doi:10.1530/eje.0.1410419)
17. Le May C, Chu K, Hu M, Ortega CS, Simpson ER, Korach KS, Tsai MJ & Mauvais-Jarvis F 2006 Estrogens protect pancreatic β-cells from apoptosis and prevent insulin-deficient diabetes mellitus inmice. PNAS 103 9232-9237. (doi:10.1073/pnas.0602956103)
18. Lenzen S 2008 Oxidative stress: the vulnerable β-cell. Biochemical Society Transactions 36 343-347. (doi:10.1042/BST0360343)
19. Lenzen S&Bailey CJ 1984 Thyroid hormones, gonadal and adrenocortical steroids and the function of the islets of Langerhans. Endocrine Reviews 5 411-434. (doi:10.1210/edrv-5-3-411)
20. Lenzen S, Nahrstedt H&Panten U 1983 Monoamine oxidase in pancreatic islets, exocrine pancreas, and liver from rats. Characterization with clorgyline, deprenyl, pargyline, tranylcypromine, and amezinium. Naunyn-Schmiedeberg's Archives of Pharmacology 324 190-195. (doi:10.1007/BF00503893)
21. Lortz S, Tiedge M, Nachtwey T, Karlsen AE, Nerup J&Lenzen S 2000 Protection of insulin-producing RINm5F cells against cytokinemediated toxicity through overexpression of antioxidant enzymes. Diabetes 49 1123-1130. (doi:10.2337/diabetes.49.7.1123)
22. Matsumoto M, Minami M, Takeda K, Sakao Y&Akira S 1996 Ectopic expression of CHOP (GADD153) induces apoptosis in M1 myeloblastic leukemia cells. FEBS Letters 395 143-147. (doi:10.1016/0014-5793 (96)01016-2)
23. Momoi T 2004 Caspases involved in ER stress-mediated cell death. Journal of Chemical Neuroanatomy 28 101-105. (doi:10.1016/j.jchemneu.2004.05.008)
24. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA&Yuan J 2000 Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-β. Nature 403 98-103. (doi:10.1038/47513)
25. Nguyen H&Syed V 2011 Progesterone inhibits growth and induces apoptosis in cancer cells through modulation of reactive oxygen species. Gynecological Endocrinology 27 830-836. (doi:10.3109/09513590.2010.538100)
26. Nicoletti I, Migliorati G, Pagliacci MC, Grignani F&Riccardi C 1991 A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. Journal of Immunological Methods 139 271-279. (doi:10.1016/0022-1759(91)90198-O)
27. Nieuwenhuizen AG, Schuiling GA, Liem SM, Moes H, Koiter TR & Uilenbroek JT 1999 Progesterone stimulates pancreatic cell proliferation in vivo. European Journal of Endocrinology 140 256-263. (doi:10.1530/eje.0.1400256)
28. Nunes VA, Gozzo AJ, Juliano MA, Cerqueira César M, Sampaio MU, Sampaio CAM&Araújo MS 2003 Antioxidant deficiency induces caspase activation in chick skeletal muscle cells. Brazilian Journal of Medical and Biological Research 36 1047-1054. (doi:10.1590/S0100-879X2003000800010)
29. Nunes VA, Gozzo AJ, Cruz-Silva I, Juliano MA, Viel TA, Godinho RO, Meirelles FV, Sampaio MU, Sampaio CA&Araujo MS 2005 Vitamin E prevents cell death induced by mild oxidative stress in chicken skeletal muscle cells. Comparative Biochemistry and Physiology C Toxicology & Pharmacology 141 225-240. (doi:10.1016/j.cca.2005.06.001)
30. Oyadomari S&Mori M 2004 Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death and Differentiation 11 381-389. (doi:10.1038/sj.cdd.4401373)
31. Pasanen S, Ylikomi T, Syvälä H&Tuohimaa P 1997 Distribution of progesterone receptor in chicken: novel target organs for progesterone and estrogen action. Molecular and Cellular Endocrinology 135 79-91. (doi:10.1016/S0303-7207(97)00192-5)
32. Picard F, Wanatabe M, Schoonjans K, Lydon J, O'Malley BW&Auwerx J 2002 Progesterone receptor-knockout mice have an improved glucose homeostasis secondary to β-cell proliferation. PNAS 99 15644-15648. (doi:10.1073/pnas.202612199)
33. Rao RV, Hermel E, Castro-Obregon S, del Rio G, Ellerby LM, Ellerby HM & Bredesen DE 2001 Coupling endoplasmic reticulum stress to the cell death program: mechanism of caspase activation. Journal of Biological Chemistry 276 33869-33874. (doi:10.1074/jbc.M102225200)
34. Rebarber A, Istwan NB, Russo-Stieglitz K, Cleary-Goldman J, Rhea DJ, Stanziano GJ&Saltzman DH 2007 Increased incidence of gestational diabetes in women receiving prophylactic 17a-hydroxyprogesterone caproate for prevention of recurrent preterm delivery. Diabetes Care 30 2277-2280. (doi:10.2337/dc07-0564)
35. Reyes MR, Sifuentes-Alvarez A&Lazalde B 2006 Estrogens are potentially the only steroids with an antioxidant role in pregnancy: in vitro evidence. Acta Obstetricia et Gynecologica Scandinavica 851090-851093. (doi:10.1080/00016340500453685)
36. Sanchez-Ramos L, Kaunitz AM&Delke I 2005 Progestational agents to prevent preterm birth: a meta-analysis of randomized controlled trials. American Journal of Obstetrics and Gynecology 105 273-279. (doi:10.1097/01.AOG.0000150559.59531.b2)
37. Scaglia L, Smith FE&Bonner-Weir S 1995 Apoptosis contributes to the involution of β-cell mass in the post partum rat pancreas. Endocrinology 136 5461-5468. (doi:10.1210/endo.136.12.7588296)
38. Scorrano L, Oakes SA, Opferman JT, Cheng EH, Sorcinelli MD, Pozzan T & Korsmeyer SJ 2003 BAX and BAK regulation of endoplasmic reticulum Ca2+: a control point for apoptosis. Science 300 135-139. (doi:10.1126/science.1081208)
39. Sen CK 1998 Redox signaling and the emerging therapeutic potential of thiol antioxidants. Biochemical Pharmacology 55 1747-1758. (doi:10.1016/S0006-2952(97)00672-2)
40. Straub SG, Sharp GW, Meglasson MD&De Souza CJ 2001 Progesterone inhibits insulin secretion by a membrane delimited, non-genomic action. Bioscience Reproduction 21 653-666. (doi:10.1023/A:1014773010350)
41. Sugaya A, Sugiyama T, Yanase S, Shen XX, Minoura H&Toyoda N 2000 Expression of glucose transporter 4 mRNA in adipose tissue and skeletal muscle of ovariectomized rats treated with sex steroid hormones. Life Sciences 66 641-648. (doi:10.1016/S0024-3205(99)00636-0)
42. Tiedge M, Lortz S, Drinkgern J&Lenzen S 1997 Relation between antioxidant enzyme gene expression and antioxidative defense status of insulin-producing cells. Diabetes 46 1733-1742. (doi:10.2337/diab.46.11.1733)
43. Toyoda Y, Miyashita T, Endo S, Tsuneyama K, Fukami T, Nakajima M & Yokoi T 2011 Estradiol and progesterone modulate halothane-induced liver injury in mice. Toxicology Letters 204 17-24. (doi:10.1016/j.toxlet.2011.03.031)
44. Verma Y&Rana SVS 2008 Effects of progesterone on benzene toxicity in rats. Archives of Industrial Hygiene and Toxicology 59 1-9. (doi:10.2478/10004-1254-59-2008-1835)
45. Wei T, Chen C, Hou J, XinW & Mori A 2000 Nitric oxide induces oxidative stress and apoptosis in neuronal cells. Biochimica et Biophysica Acta 1498 72-79. (doi:10.1016/S0167-4889(00)00078-1)
46. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, Ross AJ, Roth KA, MacGregor GR, Thompson CB&Korsmeyer SJ 2001 Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292 727-730. (doi:10.1126/science.1059108)
47. Welihinda AA&Kaufman RJ 1996 The unfolded protein response pathway in Saccharomyces cerevisiae. Oligomerization and trans-phosphorylation of Ire1p (Ern1p) are required for kinase activation. Journal of Biological Chemistry 271 18181-18187. (doi:10.1074/jbc.271.30.18181)
48. Wu J&Kaufman RJ 2006 From acute stress to physiological roles of unfolded protein response. Cell Death and Differentiation 13 374-384. (doi:10.1038/sj.cdd.4401840)
49. Xiang AH, Kawakubo M, Kjos SL&Buchanan TA 2006 Long-acting injectable progestin contraception and risk of type 2 diabetes in Latino women with prior gestational diabetes mellitus. Diabetes Care 29 613-617. (doi:10.2337/diacare.29.03.06.dc05-1940)
50. Yoshida H, Haze K, Yanagi H, Yura T&Mori K 1998 Identification of the cis-acting endoplasmic reticulum stress response element responsible for transcriptional induction of mammalian glucose-regulated proteins, Involvement of basic leucine zipper transcription factors. Journal of Biological Chemistry 273 33741-33749. (doi:10.1074/jbc.273.50.33741)
51. Zamzami N, Marchetti P, CastedoM, Decaudin D, Macho A, Hirsch T, Susin SA, Petit PX, Mignotte B&Kroemer G 1995 Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. Journal of Experimental Medicine 182 367-377. (doi:10.1084/jem.182.2.367)
52. Zhao H, Joseph J, Fales HM, Sokoloski EA, Levine RL, Vasquez-Vivar J & Kalyanaraman B 2005 Detection and characterization of the product of hydroethidine and intracellular superoxide by HPLC and limitations of fluorescence. Proceedings of National Academy of Sciences USA 102 5727-5732. (doi:10.1073/pnas.0501719102)