Death of hypothalamic astrocytes in poorly controlled diabetic rats is associated with nuclear translocation of apoptosis inducing factor

Journal of Neuroendocrinology

Volumn 20, Issue 12, 2008, Pages 1348-1360

  Garcia Caceres C ^a,b,c   Lechuga Sancho, A ^a   Argente, J ^a,b,c   Frago, L M ^a,b,c   Chowen, J A ^a,c  

^a HOSPITAL INFANTIL UNIVERSITARIO NIÑO JESÚS   (Spain)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^c Instituto de Salud Carlos III   (Spain)

Author keywords

Apoptosis; Astrocytes; Caspase

Indexed keywords

APOPTOSIS INDUCING FACTOR; CASPASE; GLIAL FIBRILLARY ACIDIC PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASTROCYTE; CELL DEATH; CELL MIGRATION; CELL STRUCTURE; CONTROLLED STUDY; DIABETES MELLITUS; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME LINKED IMMUNOSORBENT ASSAY; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; MALE; NICK END LABELING; NONHUMAN; PERIKARYON; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; WESTERN BLOTTING;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; APOPTOSIS; APOPTOSIS INDUCING FACTOR; ASTROCYTES; BCL-2-ASSOCIATED X PROTEIN; BLOOD GLUCOSE; CASPASES; DIABETES MELLITUS, EXPERIMENTAL; ENZYME ACTIVATION; GLIAL FIBRILLARY ACIDIC PROTEIN; GLYCOGEN SYNTHASE KINASE 3; HYPOTHALAMUS; IN SITU NICK-END LABELING; INSULIN; MALE; POLY(ADP-RIBOSE) POLYMERASES; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, WISTAR; TUMOR SUPPRESSOR PROTEIN P53;

EID: 56649124840     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2008.01795.x     Document Type: Article

References (59)

1. Nishikawa T, Araki E. Impact of mitochondrial ROS production in the pathogenesis of diabetes mellitus and its complications. Antioxid Redox Signal 2007; 9: 343-353.
2. Allen DA, Yaqoob MM, Harwood SM. Mechanisms of high glucose-induced apoptosis and its relationship to diabetic complications. J Nutr Biochem 2005; 16: 705-713.
3. Steger RW, Rabe MM. The effect of diabetes mellitus on endocrine and reproductive function. Proc Soc Exp Biol Med 1997; 214: 1-11.
4. Arroba AI, Frago LM, Pañeda C, Argente J, Chowen JA. The number of lactotrophs is reduced in the anterior pituitary of streptozotocin-induced diabetic rats. Diabetología 2003; 465: 634-638.
5. Lechuga-Sancho AM, Arroba AI, Frago LM, García-Cáceres C, Delgado Rúbin de Célix A, Argente J, Chowen JA. Reduction in the number of astrocytes and their projections is associated with increased synaptic protein density in the hypothalamus of poorly controlled diabetic rats. Endocrinology 2006; 147: 5314-5324.
6. Klein JP, Hains BC, Craner MJ, Black JA, Waxman SG. Apoptosis of vasopressinergic hypothalamic neurons in chronic diabetes mellitus. Neurobiol Dis 2004; 15: 221-228.
7. Garcia-Segura LM, McCarthy MM. Minireview: Role of glia in neuroendocrine function. Endocrinology 2004; 145: 1082-1086.
8. Walz W. Role of astrocytes in the clearance of excess extracellular potassium. Neurochem Int 2000; 36: 291-300.
9. Pellerin L, Bouzier-Sore AK, Aubert A, Serres S, Merle M, Costalat R, Magistretti PJ. Activity-dependent regulation of energy metabolism by astrocytes: An update. Glia 2007; 55: 1251-1262.
10. Azcoitia I, Garcia-Ovejero D, Chowen JA, Garcia-Segura LM. Astroglia play a key role in the neuroprotective actions of estrogen. Prog Brain Res 2001; 132: 469-478.
11. Ullian EM, Sapperstein SK, Christopherson KS, Barres BA. Control of synapse number by glia. Science 2001; 291: 657-660.
12. Theodosis DT, Trailin A, Poulain DA. Remodeling of astrocytes, a prerequisite for synapse turnover in the adult brain? Insights from the oxytocin system of the hypothalamus. Am J Physiol Regul Integr Comp Physiol 2006; 290: R1175-R1182.
13. Pinto S, Roseberry AG, Liu H, Diano S, Shanabrough M, Cai X, Friedman JM, Horvath TL. Rapid rewiring of arcuate nucleus feeding circuits by leptin. Science 2004; 304: 110-115.
14. Lechuga-Sancho AM, Arroba AI, Frago LM, Pañeda C, García-Cáceres C, Delgado Rubín de Célix A, Argente J, Chowen JA. Activation of the intrinsic cell death pathway, increased apoptosis and modulation of astrocytes in the cerebellum of diabetic rats. Neurobiol Dis 2006; 23: 290-299.
15. Green DR, Droemer G. The pathophysiology of mitochondrial cell death. Science 2004; 305: 626-629.
16. Wajant H. Death receptors. Essays Biochem 2003; 39: 53-71.
17. Krammer PE. CD95's deadly mission in the immune system. Nature 2000; 407: 789-795.
18. Arroba AI, Frago LM, Argente J, Chowen JA. Activation of caspase 8 in the pituitaries of streptozotocin-induced diabetic rats: Implication in increased apoptosis of lactotrophs. Endocrinology 2005 ;146: 4417-4424.
19. Arroba AI, Lechuga-Sancho AM, Frago LM, Argente J, Chowen JA. Cell-specific expression of X-linked inhibitor of apoptosis in the anterior pituitary of streptozotocin-induced diabetic rats. J Endocrinol 2007 ; 192: 215-227.
20. Hetz CA, Torres V, Quest AF. Beyond apoptosis: Nonapoptotic cell death in physiology and disease. Biochem Cell Biol 2005; 83: 579-588.
21. Krantic S, Mechawar N, Reix S, Quirion R. Apoptosis-inducing factor: A matter of neuron life and death. Prog Neurobiol 2007; 81: 179-196.
22. Srivastava RK, Srivastava AR, Korsmeyer SJ, Nesterova M, Cho-Chung YS, Longo DL. Involvement of microtubules in the regulation of Bcl2 phosphorylation and apoptosis through cyclic AMP-dependent protein kinase. Mol Cell Biol 1998; 18: 3509-3517.
23. Yenari MA, Liu J, Zheng Z, Vexler ZS, Lee JE, Giffard RG. Antiapoptotic and anti-inflammatory mechanisms of heat-shock protein protection. Ann NY Acad Sci 2005; 1053: 74-83.
24. Romero G, Liu WH, Asnaghi V, Kern TS, Lorenzi M. Activation of nuclear factor-kappaB induced by diabetes and high glucose regulates a proapoptotic program in retinal pericytes. Diabetes 2002; 51: 2241-2248.
25. Anitha M, Gondha C, Sutliff R, Parsadanian A, Mwangi S, Sitaraman SV, Srinivasan S. GDNF rescues hyperglycemia-induced diabetic enteric neuropathy through activation of the PI3K/Akt pathway. J Clin Invest 2006; 116: 344-356.
26. Ishii DN. Implication of insulin-like growth factors in the pathogenesis of diabetic neuropathy. Brain Res Brain Res Rev 1995; 20: 47-67.
27. Chen G, Goeddel DV. TNF-R1 signaling: A beautiful pathway. Science 2002; 296: 1634-1635.
28. Guillod-Maximin E, Lorsignol A, Alquier T, Pénicaud L. Acute intracarotid glucose injection towards the brain induces specific c-fos activation in hypothalamic nuclei: Involvement of astrocytes in cerebral glucose-sensing in rats. J Neuroendocrinol 2004; 16: 464-471.
29. Brown AM, Ransom BR. Astrocyte glycogen and brain energy metabolism. Glia 2007; 55: 1263-1271.
30. Xi X, Gao L, Átala DA, Smith DG, Codispoti MC, Gong B, Kern TS, Zhang JZ. Chronically elevated glucose-induced apoptosis is mediated by inactivation of Akt in cultured Müller cells. Biochem Biophys Res Commun 2005; 326: 548-553.
31. Delaney CL, Russell JW, Cheng HL, Feldman EL. Insulin-like growth factor-I and over-expression of Bcl-xL prevent glucose-mediated apoptosis in Schwann cells. J Neuropathol Exp Neurol 2001; 60: 147-160.
32. Busiguina S, Chowen JA, Argente J, Torres-Aleman I. Specific alterations of the insulin-like growth factor I system in the cerebellum of diabetic rats. Endocrinology 1996; 137: 4980-4987.
33. Al-Mashat HA, Kandru S, Liu R, Behl Y, Desta T, Graves DT. Diabetes enhances mRNA levels of proapoptotic genes and caspase activity, which contribute to impaired healing. Diabetes 2006; 55: 487-495.
34. Bojunga J, Nowak D, Mitrou PS, Hoelzer D, Zeuzem S, Chow KU. Antioxidative treatment prevents activation of death-receptor- and mitochondrion-dependent apoptosis in the hearts of diabetic rats. Diabetologia 2004; 47: 2072-2080.
35. Yan XX, Najbauer J, Woo CC, Dashtipour K, Ribak CE, Leon M. Expression of active caspase-3 in mitotic and postmitotic cells of the rat forebrain. J Comp Neurol 2001; 433: 4-22.
36. Kuranaga E, Miura M. Nonapoptotic functions of caspases: Caspases as regulatory molecules for immunity and cell-fate determination. Trends Cell Biol 2007; 17: 135-144.
37. Morishima N. Changes in nuclear morphology during apoptosis correlate with vimentin cleavage by different caspases located either upstream or downstream of Bcl-2 action. Genes Cells 1999; 4: 401-414.
38. Mouser PE, Head E, Ha KH, Rohn TT. Caspase-mediated cleavage of glial fibrillary acidic protein within degenerating astrocytes of the Alzheimer's disease brain. Am J Pathol 2006; 168: 936-946.
39. Acarin L, Villapol S, Faiz M, Rohn TT, Castellano B, González B. Caspase-3 activation in astrocytes following postnatal excitotoxic damage correlates with cytoskeletal remodeling but not with cell death or proliferation. Glia 2007; 55: 954-965.
40. Noyan-Ashraf MH, Brandizzi F, Juurlink BH. Constitutive nuclear localization of activated caspase 3 in subpopulations of the astroglial family of cells. Glia 2005; 49: 588-593.
41. Delgado-Rubín del Célix A, Chowen JA, Argente J, Frago LM. Growth hormone releasing peptide-6 acts as a survival factor in glutamate-induced excitotoxicity. J Neurochem 2006; 99: 839-849.
42. Oomman S, Strahlendorf H, Finckbone V, Strahlendorf J. Non-lethal active caspase-3 expression in Bergmann glia of postnatal rat cerebellum. Brain Res Dev Brain Res 2005; 160: 130-145.
43. Muranyi M, Ding C, He Q, Lin Y, Li PA. Streptozotocin-induced diabetes causes astrocyte death after ischemia and reperfusion injury. Diabetes 2006; 55: 349-355.
44. Stankiewicz AR, Lachapelle G, Foo CP, Radicioni SM, Mosser DD. Hsp70 inhibits heat-induced apoptosis upstream of mitochondria by preventing Bax translocation. J Biol Chem 2005; 280: 38729-38739.
45. Beurel E, Jope RS. The paradoxical pro- and anti-apoptotic actions of GSK3 in the intrinsic and extrinsic apoptosis signaling pathways. Prog Neurobiol 2006; 79: 173-189.
46. Ciccarelli R, D'Alimonte I, Ballerini P, D'Auro M, Nargi E, Buccella S, Di Iori P, Bruno V, Nicoletti F, Caciagli F. Molecular signalling mediating the protective effect of A1 adenosine and mGlu3 metabotropic glutamate receptor activation against apoptosis by oxygen/glucose deprivation in cultured astrocytes. Mol Pharmacol 2007; 71: 1369-1380.
47. Shinozaki Y, Koizumi S, Ohno Y, Nagao T, Inoue K. Extracellular ATP counteracts the ERK1/2-mediated death-promoting signaling cascades in astrocytes. Glia 2006; 54: 606-618.
48. Kawasaki T, Kitao T, Nakagawa K, Fujisaki H, Takegawa Y, Koda K, Ago Y, Baba A, Matsuda T. Nitric oxide-induced apoptosis in cultured rat astrocytes: Protection by edaravone, a radical scavenger. Glia 2007; 55: 1325-1333.
49. Redman PT, He K, Hartnett KA, Jefferson BS, Hu L, Rosenberg PA, Levitan ES, Aizenman E. Apoptotic surge of potassium currents is mediated by p38 phosphorylation of Kv2.1. Proc Natl Acad Sci USA 2007; 104: 3568-3573.
50. Wang Y, Luo W, Stricker R, Reiser G. Protease-activated receptor-1 protects rat astrocytes from apoptotic cell death via JNK-mediated release of the chemokine GRO/CINC-1. J Neurochem 2006; 98: 1046-1060.
51. Xie Z, Smith CJ, Van Eldik LJ. Activated glia induce neuron death via MAP kinase signaling pathways involving JNK and p38. Glia 2004; 45: 170-179.
52. Schechter R, Beju D, Miller KE. The effect of insulin deficiency on tau and neurofilament in the insulin knockout mouse. Biochem Biophys Res Commun 2005; 334: 979-986.
53. Price SA, Onusom L, Purves-Tyson TD, Fernyhough P, Tomlinson DR. Activation of JNK in sensory neurons protects against sensory neuron cell death in diabetes and on exposure to glucose/oxidative stress in vitro. Ann NY Acad Sci 2003; 1010: 95-99.
54. Zhou Q, Lam PY, Han D, Cadenas E. c-Jun N-terminal kinase regulates mitochondrial bioenergetics by modulating pyruvate dehydrogenase activity in primary cortical neurons. J Neurochem 2008; 104: 325-335.
55. Cao G, Clark RS, Pei W, Tin W, Zhang F, Sun FY, Grahm SH, Chen J. Translocation of apoptosis-inducing factor in vulnerable neurons after transient cerebral ishcemia and neuronal cultures after oxygen-glucose deprivation. J Cereb Blood Flow Metab 2003; 23: 1137-1150.
56. Santiago AR, Cristóvao AJ, Santos PF, Carvalho CM, Ambrósio AF. High glucose induces caspase-independent cell death in retinal neural cells. Neurobiol Dis 2007; 25: 464-472.
57. Cao G, Xing J, Xiao X, Liou AKF, Gao Y, Yin X-M, Clark RSB, Graham SH, Chen J. Critical role of calpain I in mitochondrial release of apoptosis-inducing factor in ischemic neuronal injury. J Neurosci 2007; 27: 9278-9293.
58. Kauppinen TM. Multiple roles for poly(ADP-ribose)polymerase-1 in neurological disease. Neurochem Int 2007; 50: 954-958.
59. Alano CC, Ying W, Swanson RA. Poly(ADP-ribose) polymerase-1-mediated cell death in astrocytes requires NAD+ depletion and mitochondrial permeability transition. J Biol Chem 2004; 279: 18895-18902.