Sex differences in neuroactive steroid levels in the nervous system of diabetic and non-diabetic rats

Hormones and Behavior

Volumn 57, Issue 1, 2010, Pages 46-55

  Pesaresi, Marzia ^a   Maschi, Omar ^b   Giatti, Silvia ^a   Garcia Segura, Luis Miguel ^c   Caruso, Donatella ^b   Melcangi, Roberto Cosimo ^a  

^a Pathophysiology   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c INSTITUTO CAJAL   (Spain)

Author keywords

Central nervous system; Dehydroepiandrosterone; Diabetes; Liquid chromatography tandem mass spectrometry; Neurosteroids; Peripheral nervous system; Pregnenolone; Progesterone; Rat; Testosterone

Indexed keywords

20ALPHA DIHYDROPROGESTERONE; 3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; 3BETA HYDROXY 5ALPHA PREGNAN 20 ONE; ANDROSTANEDIOL; ANDROSTANOLONE; NEUROSTEROID; PRASTERONE; PREGNENOLONE; PROGESTERONE; STREPTOZOCIN; TESTOSTERONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DISEASE; BRAIN LEVEL; BRAIN REGION; CENTRAL NERVOUS SYSTEM; CEREBELLUM; CONTROLLED STUDY; DIABETES MELLITUS; DIABETIC NEUROPATHY; FEMALE; HORMONE DETERMINATION; LIQUID CHROMATOGRAPHY; MALE; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; RAT; SCIATIC NERVE; SEX DIFFERENCE; SPINAL CORD; STREPTOZOCIN DIABETES; TANDEM MASS SPECTROMETRY;

ANIMALS; BRAIN; BRAIN DISEASES; CASE-CONTROL STUDIES; DEHYDROEPIANDROSTERONE; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEUROPATHIES; ESTROUS CYCLE; FEMALE; GONADAL STEROID HORMONES; MALE; NEUROPROTECTIVE AGENTS; PERIPHERAL NERVOUS SYSTEM; PREGNENOLONE; PROGESTERONE; RATS; RATS, SPRAGUE-DAWLEY; SEX CHARACTERISTICS; SEX FACTORS; SPINAL CORD; TESTOSTERONE;

EID: 73049086234     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2009.04.008     Document Type: Article

References (76)

1. Aaberg M.L., Burch D.M., Hud Z.R., and Zacharias M.P. Gender differences in the onset of diabetic neuropathy. J. Diabetes Complicat. 22 (2008) 83-87
2. Albers J.W., Brown M.B., Sima A.A., and Greene D.A. Nerve conduction measures in mild diabetic neuropathy in the Early Diabetes Intervention Trial: the effects of age, sex, type of diabetes, disease duration, and anthropometric factors. Tolrestat Study Group for the Early Diabetes Intervention Trial. Neurology 46 (1996) 85-91
3. Alvarez E.O., Beauquis J., Revsin Y., Banzan A.M., Roig P., De Nicola A.F., and Saravia F. Cognitive dysfunction and hippocampal changes in experimental type 1 diabetes. Behav. Brain Res. 198 (2009) 224-230
4. Andersen K., Launer L.J., Dewey M.E., Letenneur L., Ott A., Copeland J.R., Dartigues J.F., Kragh-Sorensen P., Baldereschi M., Brayne C., Lobo A., Martinez-Lage J.M., Stijnen T., and Hofman A. Gender differences in the incidence of AD and vascular dementia: the EURODEM Studies. EURODEM Incidence Research Group. Neurology 53 (1999) 1992-1997
5. Aragno M., Mastrocola R., Brignardello E., Catalano M., Robino G., Manti R., Parola M., Danni O., and Boccuzzi G. Dehydroepiandrosterone modulates nuclear factor-kappaB activation in hippocampus of diabetic rats. Endocrinology 143 (2002) 3250-3258
6. Babichev V.N., Adamskaya E.I., Kuznetsova T.A., and Shishkina I.V. Neuroendocrine control of the gonadotropic function of the hypophysis in experimental diabetes. Neurosci. Behav. Physiol. 28 (1998) 1-7
7. Backstrom T., Wahlstrom G., Wahlstrom K., Zhu D., and Wang M.D. Isoallopregnanolone; an antagonist to the anaesthetic effect of allopregnanolone in male rats. Eur. J. Pharmacol. 512 (2005) 15-21
8. Basit A., Hydrie M.Z., Hakeem R., Ahmedani M.Y., and Masood Q. Frequency of chronic complications of type II diabetes. J. Coll. Physicians Surg. Pak. 14 (2004) 79-83
9. Beauquis J., Roig P., Homo-Delarche F., De Nicola A., and Saravia F. Reduced hippocampal neurogenesis and number of hilar neurones in streptozotocin-induced diabetic mice: reversion by antidepressant treatment. Eur. J. Neurosci. 23 (2006) 1539-1546
10. Beauquis J., Saravia F., Coulaud J., Roig P., Dardenne M., Homo-Delarche F., and De Nicola A. Prominently decreased hippocampal neurogenesis in a spontaneous model of type 1 diabetes, the nonobese diabetic mouse. Exp. Neurol. 210 (2008) 359-367
11. Belelli D., and Lambert J.J. Neurosteroids: endogenous regulators of the GABA(A) receptor. Nat. Rev., Neurosci. 6 (2005) 565-575
12. Bianchi R., Buyukakilli B., Brines M., Savino C., Cavaletti G., Oggioni N., Lauria G., Borgna M., Lombardi R., Cimen B., Comelekoglu U., Kanik A., Tataroglu C., Cerami A., and Ghezzi P. Erythropoietin both protects from and reverses experimental diabetic neuropathy. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 823-828
13. Biessels G.J., and Gispen W.H. The impact of diabetes on cognition: what can be learned from rodent models?. Neurobiol. Aging 26 Suppl. 1 (2005) 36-41
14. Biessels G.J., Cristino N.A., Rutten G.J., Hamers F.P., Erkelens D.W., and Gispen W.H. Neurophysiological changes in the central and peripheral nervous system of streptozotocin-diabetic rats. Course of development and effects of insulin treatment. Brain 122 Pt 4 (1999) 757-768
15. Biessels G.J., van der Heide L.P., Kamal A., Bleys R.L., and Gispen W.H. Ageing and diabetes: implications for brain function. Eur. J. Pharmacol. 441 (2002) 1-14
16. Biessels G.J., Deary I.J., and Ryan C.M. Cognition and diabetes: a lifespan perspective. Lancet Neurol. 7 (2008) 184-190
17. Billiar R.B., Little B., Kline I., Reier P., Takaoka Y., and White R.J. The metabolic clearance rate, head and brain extractions, and brain distribution and metabolism of progesterone in the anesthetized, female monkey (Macaca mulatta). Brain Res. 94 (1975) 99-113
18. Bitran D., Hilvers R.J., and Kellogg C.K. Anxiolytic effects of 3 alpha-hydroxy-5 alpha[beta]-pregnan-20-one: endogenous metabolites of progesterone that are active at the GABAA receptor. Brain Res. 561 (1991) 157-161
19. Booya F., Bandarian F., Larijani B., Pajouhi M., Nooraei M., and Lotfi J. Potential risk factors for diabetic neuropathy: a case control study. BMC Neurol. 5 (2005) 24
20. Brown R.C., Han Z., Cascio C., and Papadopoulos V. Oxidative stress-mediated DHEA formation in Alzheimer's disease pathology. Neurobiol. Aging 24 (2003) 57-65
21. Caruso D., Scurati S., Maschi O., De Angelis L., Roglio I., Giatti S., Garcia-Segura L.M., and Melcangi R.C. Evaluation of neuroactive steroid levels by liquid chromatography-tandem mass spectrometry in central and peripheral nervous system: effect of diabetes. Neurochem. Int. 52 (2008) 560-568
22. Caruso D., Scurati S., Roglio I., Nobbio L., Schenone A., and Melcangi R.C. Neuroactive steroid levels in a transgenic rat model of CMT1A neuropathy. J. Mol. Neurosci. 34 (2008) 249-253
23. De Nicola A.F., Pietranera L., Beauquis J., Ferrini M.G., and Saravia F.E. Steroid protection in aging and age-associated diseases. Exp. Gerontol. 44 (2009) 34-40
24. Durant S., Christeff N., Coulaud J., Nunez E.A., Dardenne M., and Homo-Delarche F. Basal concentrations of various steroids in the nonobese diabetic (NOD) mouse and effect of immobilization stress. Autoimmunity 28 (1998) 249-258
25. Farace E., and Alves W.M. Do women fare worse: a metaanalysis of gender differences in traumatic brain injury outcome. J. Neurosurg. 93 (2000) 539-545
26. Franzon R., Chiarani F., Mendes R.H., Bello-Klein A., and Wyse A.T. Dietary soy prevents brain Na+, K(+)-ATPase reduction in streptozotocin diabetic rats. Diabetes Res. Clin. Pract. 69 (2005) 107-112
27. Fratiglioni L., Viitanen M., von Strauss E., Tontodonati V., Herlitz A., and Winblad B. Very old women at highest risk of dementia and Alzheimer's disease: incidence data from the Kungsholmen Project, Stockholm. Neurology 48 (1997) 132-138
28. Gee K.W., Bolger M.B., Brinton R.E., Coirini H., and McEwen B.S. Steroid modulation of the chloride ionophore in rat brain: structure-activity requirements, regional dependence and mechanism of action. J. Pharmacol. Exp. Ther. 246 (1988) 803-812
29. Gispen W.H., and Biessels G.J. Cognition and synaptic plasticity in diabetes mellitus. Trends Neurosci. 23 (2000) 542-549
30. Hedstrom H., Bixo M., Nyberg S., Spigset O., Zingmark E., and Backstrom T. Studies of pharmacokinetic and pharmacodynamic properties of isoallopregnanolone in healthy women. Psychopharmacology (Berl) 203 (2009) 85-98
31. Huang X.F., and Luu-The V. Molecular characterization of a first human 3(alpha→beta)-hydroxysteroid epimerase. J. Biol. Chem. 275 (2000) 29452-29457
32. Jacobson A.M., Samson J.A., Weinger K., and Ryan C.M. Diabetes, the brain, and behavior: is there a biological mechanism underlying the association between diabetes and depression?. Int. Rev. Neurobiol. 51 (2002) 455-479
33. Joseph E.K., and Levine J.D. Sexual dimorphism in the contribution of protein kinase C isoforms to nociception in the streptozotocin diabetic rat. Neuroscience 120 (2003) 907-913
34. Kamboj S.S., Chopra K., and Sandhir R. Neuroprotective effect of N-acetylcysteine in the development of diabetic encephalopathy in streptozotocin-induced diabetes. Metab. Brain Dis. 23 (2008) 427-443
35. Kawashima R., Kojima H., Nakamura K., Arahata A., Fujita Y., Tokuyama Y., Saito T., Furudate S., Kurihara T., Yagishita S., Kitamura K., and Tamai Y. Alterations in mRNA expression of myelin proteins in the sciatic nerves and brains of streptozotocin-induced diabetic rats. Neurochem. Res. 32 (2007) 1002-1010
36. Kaye W. Neurobiology of anorexia and bulimia nervosa. Physiol. Behav. 94 (2008) 121-135
37. Kiziltan M.E., and Benbir G. Clinical and electrophysiological differences in male and female patients with diabetic foot. Diabetes Res. Clin. Pract. 79 (2008) e17-e18
38. Kiziltan M.E., Gunduz A., Kiziltan G., Akalin M.A., and Uzun N. Peripheral neuropathy in patients with diabetic foot ulcers: clinical and nerve conduction study. J. Neurol. Sci. 258 (2007) 75-79
39. Kodl C.T., and Seaquist E.R. Cognitive dysfunction and diabetes mellitus. Endocr. Rev. 29 (2008) 494-511
40. Kohchi C., Ukena K., and Tsutsui K. Age- and region-specific expressions of the messenger RNAs encoding for steroidogenic enzymes p450scc, P450c17 and 3beta-HSD in the postnatal rat brain. Brain Res. 801 (1998) 233-238
41. Lauria G., Lombardi R., Borgna M., Penza P., Bianchi R., Savino C., Canta A., Nicolini G., Marmiroli P., and Cavaletti G. Intraepidermal nerve fiber density in rat foot pad: neuropathologic-neurophysiologic correlation. J. Peripher. Nerv. Syst. 10 (2005) 202-208
42. Leonelli E., Bianchi R., Cavaletti G., Caruso D., Crippa D., Garcia-Segura L.M., Lauria G., Magnaghi V., Roglio I., and Melcangi R.C. Progesterone and its derivatives are neuroprotective agents in experimental diabetic neuropathy: a multimodal analysis. Neuroscience 144 (2007) 1293-1304
43. Lundgren P., Stromberg J., Backstrom T., and Wang M. Allopregnanolone-stimulated GABA-mediated chloride ion flux is inhibited by 3beta-hydroxy-5alpha-pregnan-20-one (isoallopregnanolone). Brain Res. 982 (2003) 45-53
44. Marcus S.M., Kerber K.B., Rush A.J., Wisniewski S.R., Nierenberg A., Balasubramani G.K., Ritz L., Kornstein S., Young E.A., and Trivedi M.H. Sex differences in depression symptoms in treatment-seeking adults: confirmatory analyses from the Sequenced Treatment Alternatives to Relieve Depression study. Compr. Psychiatry 49 (2008) 238-246
45. Marx C.E., Trost W.T., Shampine L.J., Stevens R.D., Hulette C.M., Steffens D.C., Ervin J.F., Butterfield M.I., Blazer D.G., Massing M.W., and Lieberman J.A. The neurosteroid allopregnanolone is reduced in prefrontal cortex in Alzheimer's disease. Biol. Psychiatry 60 (2006) 1287-1294
46. Mastrocola R., Restivo F., Vercellinatto I., Danni O., Brignardello E., Aragno M., and Boccuzzi G. Oxidative and nitrosative stress in brain mitochondria of diabetic rats. J. Endocrinol. 187 (2005) 37-44
47. McCall A.L. Diabetes mellitus and the central nervous system. Int. Rev. Neurobiol. 51 (2002) 415-453
48. Meffre D., Delespierre B., Gouezou M., Schumacher M., Stein D.G., and Guennoun R. 3beta-Hydroxysteroid dehydrogenase/5-ene-4-ene isomerase mRNA expression in rat brain: effect of pseudopregnancy and traumatic brain injury. J. Steroid Biochem. Mol. Biol. 104 (2007) 293-300
49. Meffre D., Pianos A., Liere P., Eychenne B., Cambourg A., Schumacher M., Stein D.G., and Guennoun R. Steroid profiling in brain and plasma of male and pseudopregnant female rats after traumatic brain injury: analysis by gas chromatography/mass spectrometry. Endocrinology 148 (2007) 2505-2517
50. Melcangi R.C., and Panzica G.C. Neuroactive steroids: old players in a new game. Neuroscience 138 (2006) 733-739
51. Melcangi R.C., Garcia-Segura L.M., and Mensah-Nyagan A.G. Neuroactive steroids: state of the art and new perspectives. Cell. Mol. Life Sci. 65 (2008) 777-797
52. Mellon S.H., and Deschepper C.F. Neurosteroid biosynthesis: genes for adrenal steroidogenic enzymes are expressed in the brain. Brain Res. 629 (1993) 283-292
53. Meyer L., Venard C., Schaeffer V., Patte-Mensah C., and Mensah-Nyagan A.G. The biological activity of 3alpha-hydroxysteroid oxido-reductase in the spinal cord regulates thermal and mechanical pain thresholds after sciatic nerve injury. Neurobiol. Dis. 30 (2008) 30-41
54. Naik A.K., Pathirathna S., and Jevtovic-Todorovic V. GABA(A) receptor modulation in dorsal root ganglia in vivo affects chronic pain after nerve injury. Neuroscience 154 (2008) 1539-1553
55. Niemeier J.P., Marwitz J.H., Lesher K., Walker W.C., and Bushnik T. Gender differences in executive functions following traumatic brain injury. Neuropsychol. Rehabil. 17 (2007) 293-313
56. Nitta A., Murai R., Suzuki N., Ito H., Nomoto H., Katoh G., Furukawa Y., and Furukawa S. Diabetic neuropathies in brain are induced by deficiency of BDNF. Neurotoxicol. Teratol. 24 (2002) 695-701
57. Pathirathna S., Brimelow B.C., Jagodic M.M., Krishnan K., Jiang X., Zorumski C.F., Mennerick S., Covey D.F., Todorovic S.M., and Jevtovic-Todorovic V. New evidence that both T-type calcium channels and GABAA channels are responsible for the potent peripheral analgesic effects of 5alpha-reduced neuroactive steroids. Pain 114 (2005) 429-443
58. Pathirathna S., Todorovic S.M., Covey D.F., and Jevtovic-Todorovic V. 5alpha-reduced neuroactive steroids alleviate thermal and mechanical hyperalgesia in rats with neuropathic pain. Pain 117 (2005) 326-339
59. Roglio I., Bianchi R., Giatti S., Cavaletti G., Caruso D., Scurati S., Crippa D., Garcia-Segura L.M., Camozzi F., Lauria G., and Melcangi R.C. Testosterone derivatives are neuroprotective agents in experimental diabetic neuropathy. Cell. Mol. Life Sci. 64 (2007) 1158-1168
60. Salonia A., Lanzi R., Scavini M., Pontillo M., Gatti E., Petrella G., Licata G., Nappi R.E., Bosi E., Briganti A., Rigatti P., and Montorsi F. Sexual function and endocrine profile in fertile women with type 1 diabetes. Diabetes Care 29 (2006) 312-316
61. Saravia F., Revsin Y., Lux-Lantos V., Beauquis J., Homo-Delarche F., and De Nicola A.F. Oestradiol restores cell proliferation in dentate gyrus and subventricular zone of streptozotocin-diabetic mice. J. Neuroendocrinol. 16 (2004) 704-710
62. Saravia F.E., Beauquis J., Revsin Y., Homo-Delarche F., de Kloet E.R., and De Nicola A.F. Hippocampal neuropathology of diabetes mellitus is relieved by estrogen treatment. Cell. Mol. Neurobiol. 26 (2006) 943-957
63. Simonds V.M., and Whiffen V.E. Are gender differences in depression explained by gender differences in co-morbid anxiety?. J. Affect Disord. 77 (2003) 197-202
64. Steen E., Terry B.M., Rivera E.J., Cannon J.L., Neely T.R., Tavares R., Xu X.J., Wands J.R., and de la Monte S.M. Impaired insulin and insulin-like growth factor expression and signaling mechanisms in Alzheimer's disease-is this type 3 diabetes?. J. Alzheimers Dis. 7 (2005) 63-80
65. Stranahan A.M., Arumugam T.V., Cutler R.G., Lee K., Egan J.M., and Mattson M.P. Diabetes impairs hippocampal function through glucocorticoid-mediated effects on new and mature neurons. Nat. Neurosci. 11 (2008) 309-317
66. Sugimoto K., Murakawa Y., and Sima A.A. Diabetic neuropathy-a continuing enigma. Diabetes Metab. Res. Rev. 16 (2000) 408-433
67. Tanaka M., Nakaya S., Kumai T., Watanabe M., Matsumoto N., and Kobayashi S. Impaired testicular function in rats with diet-induced hypercholesterolemia and/or streptozotocin-induced diabetes mellitus. Endocr. Res. 27 (2001) 109-117
68. van Dam E.W., Dekker J.M., Lentjes E.G., Romijn F.P., Smulders Y.M., Post W.J., Romijn J.A., and Krans H.M. Steroids in adult men with type 1 diabetes: a tendency to hypogonadism. Diabetes Care 26 (2003) 1812-1818
69. Veiga S., Leonelli E., Beelke M., Garcia-Segura L.M., and Melcangi R.C. Neuroactive steroids prevent peripheral myelin alterations induced by diabetes. Neurosci. Lett. 402 (2006) 150-153
70. Vinik A.I., Park T.S., Stansberry K.B., and Pittenger G.L. Diabetic neuropathies. Diabetologia 43 (2000) 957-973
71. Wang M., He Y., Eisenman L.N., Fields C., Zeng C.M., Mathews J., Benz A., Fu T., Zorumski E., Steinbach J.H., Covey D.F., Zorumski C.F., and Mennerick S. 3beta-hydroxypregnane steroids are pregnenolone sulfate-like GABA(A) receptor antagonists. J. Neurosci. 22 (2002) 3366-3375
72. Watzka M., Bidlingmaier F., Schramm J., Klingmuller D., and Stoffel-Wagner B. Sex- and age-specific differences in human brain CYP11A1 mRNA expression. J. Neuroendocrinol. 11 (1999) 901-905
73. Weill-Engerer S., David J.P., Sazdovitch V., Liere P., Eychenne B., Pianos A., Schumacher M., Delacourte A., Baulieu E.E., and Akwa Y. Neurosteroid quantification in human brain regions: comparison between Alzheimer's and nondemented patients. J. Clin. Endocrinol. Metab. 87 (2002) 5138-5143
74. Yagihashi S. Pathogenetic mechanisms of diabetic neuropathy: lessons from animal models. J. Peripher. Nerv. Syst. 2 (1997) 113-132
75. Yorek M.A., Coppey L.J., Gellett J.S., Davidson E.P., Bing X., Lund D.D., and Dillon J.S. Effect of treatment of diabetic rats with dehydroepiandrosterone on vascular and neural function. Am. J. Physiol., Endocrinol. Metab. 283 (2002) E1067-E1075
76. Zhang W.J., Tan Y.F., Yue J.T., Vranic M., and Wojtowicz J.M. Impairment of hippocampal neurogenesis in streptozotocin-treated diabetic rats. Acta Neurol. Scand. 117 (2008) 205-210