Sensory neurons derived from diabetic rats have diminished internal Ca2+ stores linked to impaired re-uptake by the endoplasmic reticulum

ASN Neuro

Volumn 4, Issue 1, 2012, Pages 1-10

  Zherebitskaya, Elena ^a   Schapansky, Jason ^a,b   Akude, Eli ^a,b   Smith, Darrell R ^a,b   van der Ploeg, Randy ^a   Solovyova, Natasha ^c   Verkhratsky, Alexei ^c   Fernyhough, Paul ^a,b  

^a ST BONIFACE GENERAL HOSPITAL   (Canada)

^b UNIVERSITY OF MANITOBA   (Canada)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Axon plasticity; Diabetic neuropathy; Dorsal root ganglia (DRG); Neurodegeneration

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); CALCIUM; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; MALE; NONHUMAN; PROTEIN EXPRESSION; RAT; SARCOPLASMIC RETICULUM; SENSORY NERVE CELL; WESTERN BLOTTING; ANIMAL; EXPERIMENTAL DIABETES MELLITUS; IMMUNOHISTOCHEMISTRY; METABOLISM; PATCH CLAMP; SENSORY RECEPTOR; SPRAGUE DAWLEY RAT;

ANIMALS; BLOTTING, WESTERN; CALCIUM; DIABETES MELLITUS, EXPERIMENTAL; ENDOPLASMIC RETICULUM; IMMUNOHISTOCHEMISTRY; MALE; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; SENSORY RECEPTOR CELLS;

EID: 84863232810     PISSN: None     EISSN: 17590914     Source Type: Journal    
DOI: 10.1042/AN20110038     Document Type: Article

References (59)

1. 2+ storage. Cardiovasc Res 70:346-353.
2. Akude E, Zherebitskaya E, Chowdhury SK, Smith DR, Dobrowsky RT, Fernyhough P (2011) Diminished superoxide generation is associated with respiratory chain dysfunction and changes in the mitochondrial proteome of sensory neurons from diabetic rats. Diabetes 60:288-297.
3. Akude E, Zherebitskaya E, Roy Chowdhury SK, Girling K, Fernyhough P (2010) 4-Hydroxy-2-nonenal induces mitochondrial dysfunction and aberrant axonal outgrowth in adult sensory neurons that mimics features of diabetic neuropathy. Neurotox Res 17:28-38.
4. Beiswenger KK, Calcutt NA, Mizisin AP (2008) Dissociation of thermal hypoalgesia and epidermal denervation in streptozotocin-diabetic mice. Neurosci Lett 442:267-272.
5. Borge PD Jr., Wolf BA (2003) Insulin receptor substrate 1 regulation of sarcoendoplasmic reticulum calcium ATPase 3 in insulin-secreting beta-cells. J Biol Chem 278:11359-11368.
6. Burdakov D, Petersen OH, Verkhratsky A (2005) Intraluminal calcium as a primary regulator of endoplasmic reticulum function. Cell Calcium 38:303-310.
7. Chowdhury SK, Zherebitskaya E, Smith DR, Akude E, Chattopadhyay S, Jolivalt CG, Calcutt NA, Fernyhough P (2010) Mitochondrial respiratory chain dysfunction in dorsal root ganglia of streptozotocin-induced diabetic rats and its correction by insulin treatment. Diabetes 59:1082-1091.
8. Christianson JA, Riekhof JT, Wright DE (2003) Restorative effects of neurotrophin treatment on diabetes-induced cutaneous axon loss in mice. Exp Neurol 179:188-199.
9. Christianson JA, Ryals JM, Johnson MS, Dobrowsky RT, Wright DE (2007) Neurotrophic modulation of myelinated cutaneous innervation and mechanical sensory loss in diabetic mice. Neuroscience 145:303-313.
10. Coleman M (2005) Axon degeneration mechanisms: commonality amid diversity. Nat Rev Neurosci 6:889-898.
11. Ebenezer GJ, O'Donnell R, Hauer P, Cimino NP, McArthur JC, Polydefkis M (2011) Impaired neurovascular repair in subjects with diabetes following experimental intracutaneous axotomy. Brain 134:1853-1863.
12. Fernyhough P, Gallagher A, Averill SA, Priestley JV, Hounsom L, Patel J, Tomlinson DR (1999) Aberrant neurofilament phosphorylation in sensory neurons of rats with diabetic neuropathy. Diabetes 48:881-889.
13. Fernyhough P, Huang TJ, Verkhratsky A (2003) Mechanism of mitochondrial dysfunction in diabetic sensory neuropathy. J Peripher Nerv Syst 8:227-235.
14. Francis G, Martinez J, Liu W, Nguyen T, Ayer A, Fine J, Zochodne D, Hanson LR, Frey WH II, Toth C (2009) Intranasal insulin ameliorates experimental diabetic neuropathy. Diabetes 58:934-945.
15. Glazner GW, Fernyhough P (2002) Neuronal survival in the balance: are endoplasmic reticulum membrane proteins the fulcrum? Cell Calcium 32:421-433.
16. Gruszczynska-Biegala J, Pomorski P, Wisniewska MB, Kuznicki J (2011) Differential roles for STIM1 and STIM2 in store-operated calcium entry in rat neurons. PLoS ONE 6:e19285.
17. Hall KE, Liu J, Sima AA, Wiley JW (2001) Impaired inhibitory G-protein function contributes to increased calcium currents in rats with diabetic neuropathy. J Neurophysiol 86:760-770.
18. Hall KE, Sima AA, Wiley JW (1995) Voltage-dependent calcium currents are enhanced in dorsal root ganglion neurones from the Bio Bred/Worchester diabetic rat. J Physiol 486 (Pt 2):313-322.
19. Hardingham GE, Arnold FJ, Bading H (2001) Nuclear calcium signaling controls CREB-mediated gene expression triggered by synaptic activity. Nat Neurosci 4:261-267.
20. Hoke A, Morris M, Haughey NJ (2009) GPI-1046 protects dorsal root ganglia from gp120-induced axonal injury by modulating store-operated calcium entry. J Peripher Nerv Syst 14:27-35.
21. Huang TJ, Price SA, Chilton L, Calcutt NA, Tomlinson DR, Verkhratsky A, Fernyhough P (2003) Insulin prevents depolarization of the mitochondrial inner membrane in sensory neurons of type 1 diabetic rats in the presence of sustained hyperglycemia. Diabetes 52:2129-2136.
22. Huang TJ, Sayers NM, Fernyhough P, Verkhratsky A (2002) Diabetes-induced alterations in calcium homeostasis in sensory neurones of streptozotocin-diabetic rats are restricted to lumbar ganglia and are prevented by neurotrophin-3. Diabetologia 45:560-570.
23. Huang TJ, Sayers NM, Verkhratsky A, Fernyhough P (2005a) Neurotrophin-3 prevents mitochondrial dysfunction in sensory neurons of streptozotocindiabetic rats. Exp Neurol 194:279-283.
24. Huang TJ, Verkhratsky A, Fernyhough P (2005b) Insulin enhances mitochondrial inner membrane potential and increases ATP levels through phosphoinositide 3-kinase in adult sensory neurons. Mol Cell Neurosci 28:42-54.
25. Jolivalt CG, Lee CA, Ramos KM, Calcutt NA (2008) Allodynia and hyperalgesia in diabetic rats are mediated by GABA and depletion of spinal potassiumchloride co-transporters. Pain 140:48-57.
26. Kennedy WR, Wendelschafer-Crabb G, Johnson T (1996) Quantitation of epidermal nerves in diabetic neuropathy. Neurology 47:1042-1048.
27. Kilinc D, Gallo G, Barbee KA (2009) Mechanical membrane injury induces axonal beading through localized activation of calpain. Exp Neurol 219:553-561.
28. Knoferle J, Koch JC, Ostendorf T, Michel U, Planchamp V, Vutova P, Tonges L, Stadelmann C, Bruck W, Bahr M et al. (2010) Mechanisms of acute axonal degeneration in the optic nerve in vivo. Proc Natl Acad Sci USA 107:6064-6069.
29. Kostyuk E, Pronchuk N, Shmigol A (1995) Calcium signal prolongation in sensory neurones of mice with experimental diabetes. Neuroreport 6:1010-1012.
30. Kostyuk E, Voitenko N, Kruglikov I, Shmigol A, Shishkin V, Efimov A, Kostyuk P (2001) Diabetes-induced changes in calcium homeostasis and the effects of calcium channel blockers in rat and mice nociceptive neurons. Diabetologia 44:1302-1309.
31. Kruglikov I, Gryshchenko O, Shutov L, Kostyuk E, Kostyuk P, Voitenko N (2004) Diabetes-induced abnormalities in ER calcium mobilization in primary and secondary nociceptive neurons. Pflugers Arch 448:395-401.
32. Llano I, Gonzalez J, Caputo C, Lai FA, Blayney LM, Tan YP, Marty A (2000) Presynaptic calcium stores underlie large-amplitude miniature IPSCs and spontaneous calcium transients. Nat Neurosci 3:1256-1265.
33. Malik RA, Tesfaye S, Newrick PG, Walker D, Rajbhandari SM, Siddique I, Sharma AK, Boulton AJ, King RH, Thomas PK et al. (2005) Sural nerve pathology in diabetic patients with minimal but progressive neuropathy. Diabetologia 48:578-585.
34. Mattson MP, Gary DS, Chan SL, Duan W (2001) Perturbed endoplasmic reticulum function, synaptic apoptosis and the pathogenesis of Alzheimer's disease. Biochem Soc Symp 67:151-162.
35. Mizisin AP, Nelson RW, Sturges BK, Vernau KM, Lecouteur RA, Williams DC, Burgers ML, Shelton GD (2007) Comparable myelinated nerve pathology in feline and human diabetes mellitus. Acta Neuropathol 113:431-442.
36. Paschen W, Frandsen A (2001) Endoplasmic reticulum dysfunction - a common denominator for cell injury in acute and degenerative diseases of the brain? J Neurochem 79:719-725.
37. 2+ signalling by NAADP. Trends Biochem Sci 26:482-489.
38. Patil C, Walter P (2001) Intracellular signaling from the endoplasmic reticulum to the nucleus: the unfolded protein response in yeast and mammals. Curr Opin Cell Biol 13:349-355.
39. 2+ stores? Trends Neurosci 24:271-276.
40. Quattrini C, Tavakoli M, Jeziorska M, Kallinikos P, Tesfaye S, Finnigan J, Marshall A, Boulton AJ, Efron N, Malik RA (2007) Surrogate markers of small fiber damage in human diabetic neuropathy. Diabetes 56:2148-2154.
41. Rose CR, Konnerth A (2001) Stores not just for storage. intracellular calcium release and synaptic plasticity. Neuron 31:519-522.
42. Schmidt RE, Dorsey D, Parvin CA, Beaudet LN, Plurad SB, Roth KA (1997) Dystrophic axonal swellings develop as a function of age and diabetes in human dorsal root ganglia. J Neuropathol Exp Neurol 56:1028-1043.
43. 2+ release. Trends Pharmacol Sci 16:386-391.
44. Solovyova N, Verkhratsky A (2002) Monitoring of free calcium in the neuronal endoplasmic reticulum: an overview of modern approaches. J Neurosci Methods 122:1-12.
45. 2+ entry. EMBO J 21:622-630.
46. Stys PK (2005) General mechanisms of axonal damage and its prevention. J Neurol Sci 233:3-13.
47. 2+ release channels: does diversity in form equal diversity in function? Physiol Rev 76:1027-1071.
48. 3 receptor isoforms by endogenous modulators. Trends Pharmacol Sci 22:580-586.
49. Towns R, Kabeya Y, Yoshimori T, Guo C, Shangguan Y, Hong S, Kaplan M, Klionsky DJ, Wiley JW (2005) Sera from patients with type 2 diabetes and neuropathy induce autophagy and colocalization with mitochondria in SY5Y cells. Autophagy 1:163-170.
50. Verkhratsky A (2005) Physiology and pathophysiology of the calcium store in the endoplasmic reticulum of neurons. Physiol Rev 85:201-279.
51. 2+ dyshomeostasis drive neuronal pathology in diabetes. Cell Calcium 44: 112-122.
52. Verkhratsky A, Petersen OH (2002) The endoplasmic reticulum as an integrating signalling organelle: from neuronal signalling to neuronal death. Eur J Pharmacol 447:141-154.
53. Verkhratsky A, Toescu EC (1998) Calcium and neuronal ageing. Trends Neurosci 21:2-7.
54. Voitenko NV, Kostyuk EP, Kruglikov IA, Kostyuk PG (1999) Changes in calcium signalling in dorsal horn neurons in rats with streptozotocin-induced diabetes. Neuroscience 94:887-890.
55. Voitenko NV, Kruglikov IA, Kostyuk EP, Kostyuk PG (2000) Effect of streptozotocin-induced diabetes on the activity of calcium channels in rat dorsal horn neurons. Neuroscience 95:519-524.
56. Yagihashi S (1996) Pathology and pathogenetic mechanisms of diabetic neuropathy. Diabetes Metab Rev 11:193-225.
57. 2+ elevation, missorting of endogenous Tau into dendrites, Tau phosphorylation, and destruction of microtubules and spines. J Neurosci 30:11938-11950.
58. Zheng JQ, Kelly TK, Chang B, Ryazantsev S, Rajasekaran AK, Martin KC, Twiss JL (2001) A functional role for intra-axonal protein synthesis during axonal regeneration from adult sensory neurons. J Neurosci 21:9291-9303.
59. Zherebitskaya E, Akude E, Smith DR, Fernyhough P (2009) Development of selective axonopathy in adult sensory neurons isolated from diabetic rats: role of glucose-induced oxidative stress. Diabetes 58:1356-1364.