NAD+-CONVERTING ENZYMES IN NEURONAL AND GLIAL CELLS: CD38 AS A NOVEL TARGET FOR NEUROPROTECTION

Cover Page


Cite item

Full Text

Abstract

The review contains current data on molecular mechanisms which control NAD+ homeostasis in brain cells. It also deals with the role of NAD+-converting enzymes in regulation of functional activity, viability and intercellular communication of neuronal and glial cells. Special attention is paid to involvement of CD38 into regulation of NAD+ levels in brain cells in normal and pathological conditions.

 

Keywords

About the authors

A. B. Salmina

Krasnoyarsk State Medical University named after Professor V.F. Voino-Yasenetsky, Ministry of Public Health and Social Development, Russian Federation

Author for correspondence.
Email: allasalmina@mail.ru
доктор медицинских наук, профессор, заведующая кафедрой биохимии с курсами меди- цинской, фармацевтической и токсикологической химии, проректор по инновационному развитию и междуна- родной деятельности ГБОУ ВПО КрасГМУ им. проф. В.Ф. Войно-Ясенецкого Адрес: 660022, Красноярск, ул. П. Железняка, д. 1 Тел.: (391) 228-07-69 Russian Federation

A. I. Inzhutova

Krasnoyarsk State Medical University named after Professor V.F. Voino-Yasenetsky, Ministry of Public Health and Social Development, Russian Federation

Email: a_morgun@mail.ru
кандидат медицинских наук, научный сотрудник НИИ молекулярной медицины и патобиохимии, старший преподаватель кафедры биохимии с курсами медицинской, фармацевтической и токсико- логической химии ГБОУ ВПО КрасГМУ им. проф. В.Ф. Войно-Ясенецкого Адрес: 660022, Красноярск, ул. П. Железняка, д. 1 Russian Federation

A. V. Morgun

Krasnoyarsk State Medical University named after Professor V.F. Voino-Yasenetsky, Ministry of Public Health and Social Development, Russian Federation

Email: a_morgun@mail.ru
кандидат медицинских наук, ассистент кафедры педатрии ИПО ГБОУ ВПО КрасГМУ им. проф. В.Ф. Войно-Ясенецкого Адрес: 660022, Красноярск, ул. П. Железняка, д. 1 Тел.: (391) 243-39-52 Russian Federation

O. S. Okuneva

Krasnoyarsk State Medical University named after Professor V.F. Voino-Yasenetsky, Ministry of Public Health and Social Development, Russian Federation

Email: olesyaokuneva@gmail.com
кандидат медицинских наук, старший преподаватель кафедры биохимии с курсами меди- цинской, фармацевтической и токсикологической химии, ГБОУ ВПО КрасГМУ им. проф. В.Ф. Войно-Ясенецкого Адрес: 660022, Красноярск, ул. П. Железняка, д. 1 Тел.: (391) 228-07-69 Russian Federation

N. A. Malinovskaya

Krasnoyarsk State Medical University named after Professor V.F. Voino-Yasenetsky, Ministry of Public Health and Social Development, Russian Federation

Email: konsuelo81@mail.ru
кандидат медицинских наук, доцент кафедры биохимии с курсами медицин- ской, фармацевтической и токсикологической химии, научный сотрудник НИИ молекулярной медицины и пато- биохимии ГБОУ ВПО КрасГМУ им. проф. В.Ф. Войно-Ясенецкого Адрес: 660022, Красноярск, ул. П. Железняка, д. 1 Тел.: (391) 228-07-69 Russian Federation

O. L. Lopatina

Krasnoyarsk State Medical University named after Professor V.F. Voino-Yasenetsky, Ministry of Public Health and Social Development, Russian Federation

Email: ol.lopatina@gmail.com
кандидат медицинских наук, старший преподаватель кафедры биохимии с курсами медицинской, фармацевтической и токсикологической химии, ГБОУ ВПО КрасГМУ им. проф. В.Ф. Войно- Ясенецкого Адрес: 660022, Красноярск, ул. П. Железняка, д. 1 Тел.: (391) 228-07-69 Russian Federation

M. M. Petrova

Krasnoyarsk State Medical University named after Professor V.F. Voino-Yasenetsky, Ministry of Public Health and Social Development, Russian Federation

Email: stk99@yandex.ru
доктор медицинских наук, профессор, заведующая кафедрой поликлинической терапии и семейной медицины, проректор по научной работе ГБОУ ВПО КрасГМУ им. проф. В.Ф. Войно- Ясенецкого Адрес: 660022, Красноярск, ул. П. Железняка, д. 1 Тел.: (391) 228-07-69 Russian Federation

T. E. Taranunushenko

Krasnoyarsk State Medical University named after Professor V.F. Voino-Yasenetsky, Ministry of Public Health and Social Development, Russian Federation

Email: tetar@rambler.ru
доктор медицинских наук, профессор, заведующая кафедрой педиатрии ИПО ГБОУ ВПО КрасГМУ им. проф. В.Ф. Войно-Ясенецкого Адрес: 660022, Красноярск, ул. П. Железняка, д. 1 Тел.: (391) 243-39-52 Russian Federation

A. A. Fursov

Krasnoyarsk State Medical University named after Professor V.F. Voino-Yasenetsky, Ministry of Public Health and Social Development, Russian Federation

Email: fursov_alex@mail.ru
кандидат медицинских наук, ассистент кафедры анестезиологии и реаниматологии ГБОУ ВПО КрасГМУ им. проф. В.Ф. Войно-Ясенецкого Адрес: 660022, Красноярск, ул. П. Железняка, д. 1 Тел.: (391) 2283468 Russian Federation

N. V. Kuvacheva

Krasnoyarsk State Medical University named after Professor V.F. Voino-Yasenetsky, Ministry of Public Health and Social Development, Russian Federation

Email: natalya.kuvacheva@gmail.com
During writing this review, the authors have been supporting by the grant of the Federal Program «Scientific and pedagogical specialists of innovative Russia» (N 8061, 2012–2013). Russian Federation

References

  1. Doyle K.P, Simon R.P., Stenzel-Poore M.P. Mechanisms of ischemic brain damage. Neuropharmacology. 2008; 55 (3): 310–318.
  2. Houtkooper R.H., Canto C., Wanders R.J., Auwerx J. The secret life of NAD+: an old metabolite controlling new metabolic signaling pathways. Endocrine Reviews. 2010; 31 (2): 194–223.
  3. Salmina A.B. Neuron-glia interactions as therapeutic target in neurodegeneration. J. Alzheimer’s Disease. 2009; 16 (4): 485–502.
  4. Virag, L., Szabo C. The therapeutic potential of poly(ADP-ribose) polymerase inhibitors. Pharmacol. Rev. 2002; 54: 375–430.
  5. Soane L., Kahraman S., Kristian T., Fiskum G. Mechanisms of impaired mitochondrial energy metabolism in acute and chronic neurodegenerative disorders. J. Neurosci. Res. 2007; 85 (15): 3407–3415.
  6. Billington R.A., Travelli C., Ercolano E., Galli U., Roman C.B., Grolla A.A., Canonico P.L., Condorelli F., Genazzani A.A. Characterization of NAD+ uptake in mammalian cells. J. Biol. Chem. 2008; 283 (10): 6367–6374.
  7. Magni G., Amici A., Emanuelli M., Orsomando G., Raffaelli N., Ruggieri S. Enzymology of NAD+ homeostasis in man. Cell. Mol. Life Sci. 2004; 61: 19–34.
  8. Kim M.Y., Zhang T., Kraus W.L. Poly(ADP-ribosyl)ation by PARP1: «PAR-laying» NAD+ into a nuclear signal. Genes & Development. 2005; 19: 1951–1967.
  9. Komjáti K., Besson V.C., Szabó C. Poly (ADP-ribose) polymerase inhibitors as potential therapeutic agents in stroke and neurotrauma. Curr Drug Targets CNS Neurol. Disord. 2005; 4 (2): 179–194.
  10. Moroni F, Chiarugi A. Post-ischemic brain damage: targeting PARP-1 within the ischemic neurovascular units as a realistic avenue to stroke treatment. FEBS J. 2009; 276 (1): 36–45.
  11. Min W., Wang Z.Q. Poly (ADP-ribose) glycohydrolase (PARP) and its therapeutic potential. Front. Biosci. 2009; 1 (14): 1619–1626.
  12. Malavasi F., Deaglio S., Funaro A., Ferrero E., Horenstein A.L., Ortolan E., Vaisitti T., Aydin S. Evolution and function of the ADP cibosyl cyclase/CD38 gene family in physiology and pathology. Physiol. Rev. 2008; 88: 841–886.
  13. Higashida H., Yokoyama S., Kikuchi M., Munesue T. CD38 and its role in oxytocin secretion and social behavior. Hormones and Behavior. 2012; 61: 351–358.
  14. Higashida H., Salmina A.B., Olovyannikova R.Ya., Hashii M., Yokoyama S., Koizumi K., Jin D., Liu H.X., Lopatina O., Amina S., Islam M.S., Huang J.J., Noda M. Cyclic ADP-ribose as a universal calcium signal molecule in the nervous system. Neurochem. Int. 2007; 51: 192–199.
  15. Cakir-Kiefer C, Muller-Steffner H., Oppenheimer N., Schuber F. Kinetic competence of the cADP-ribose-CD38 complex as an intermediate in the CD38/NAD+ glycohydrolase-catalysed reactions: implication for CD38 signaling. Biochem. J. 2001; 358: 399–406.
  16. Hashii M, Shuto S, Fukuoka M., Kudoh T, Matsuda A, Higashida H. Amplification of depolarization-induced and ryanodine-sensitive cytosolic Ca2+ elevation by synthetic carbocyclic analogs of cyclic ADP-ribose and their antagonistic effects in NG108-15 neuronal cells. J. Neurochem. 2005; 94 (2): 316–323.
  17. Higashida H., Hashii M., Yokoyama S., Hoshi N., Chen X.L., Egorova A., Noda M., Zhang J.S. Cyclic ADP-ribose as a second messenger revisited from a new aspect of signal transduction from receptors to ADP-ribosyl cyclase. Pharmacology and Therapeutics. 2001; 90: 283–296.
  18. Higashida H., Hashii M., Yokoyama S., Hoshi N., Asai K., Kato T. Cyclic ADP-ribose as a potential second messenger for neuronal Ca2+ signaling. J. Neurochemistry. 2001; 76: 321–331.
  19. Ceni C., Pochon N., Villaz M., Muller-Steffner H., Schuber F., Baratier J., De Waard M., Ronjat M., Moutin M.J. The CD38-independent ADP-ribosyl cyclase from mouse brain synaptosomes: a comparative study of neonate and adult brain. Biochem. J. 2006; 395: 417–426.
  20. Salmina A.B., Okuneva O.S., Malinovskaya N.A., Taranushenko T.E., Morgun A.V., Mantorova N.S., Mikhutkina S.V. NAD+-dependent mechanisms of disturbances of viability of brain cells during the acute period of hypoxic-ischemic perinatal injury. J. Neurochem. 2008; 2 (3): 215–221.
  21. Higashida H., Zhang J.S., Mochida S., Chen X.L., Shin Y., Noda M., Hossain K.Z., Hoshi N., Hashii M., Shigemoto R., Nakanishi S., Fukuda Y., Yokoyama S. Subtype-specific coupling with ADP-ribosyl cyclase of metabotropic glutamate receptors in retina, cervical superior ganglion andNG108-15 cells. J. Neurochem. 2003; 85: 1148–1158.
  22. Noda M., Yasuda S., Okada M., Higashida H., Shimada A., Iwata N., Ozaki N., Nishikawa K., Shirasawa S., Uchida M., Aoki S., Wada K. Recombinant human 5-HT5A receptors stably expressed in C6 glioma cells couple to multiple signal transduction pathways. J. Neurochem. 2003; 84: 222–232.
  23. Wilson H.L., Dipp M., Thomas J.T., Lad C., Galione A., Evans A.M. ADP-ribosyl cyclase and cyclic ADP-ribose hydrolase act as redox sensors. J. Biol. Chem. 2001; 276: 1180–1188.
  24. Sun L.A., Adebanjo O.A., Koval A., Anandatheerthavarada H.K., Iqbal J., Wu X.Y., Moonga B.S., Wu X.B., Biswas G., Bevis P.J., Kumegawa M., Epstein S., Huang C.L., Avadhani N.G., Abe E., Zaidi M. Novel mechanism for coupling cellular intermediary metabolism to cytosolic Ca2+ signaling via CD38/ADP-ribosyl cyclase a putative intracellular NAD+ sensor. FASEB J. 2002; 16: 302–314.
  25. Ceni C., Muller-Steffner H., Lund F., Pochon N., Schweitzer A., De Waard M., Schuber F., Villaz M., Moutin M.J. Evidence for an intracellular ADP-ribosyl cyclase/NAD+-glycohydrolase in brain from CD38-deficient mice. J. Biol. Chem. 2003; 278 (42): 40670–40678.
  26. Ma Y., Chen H., He X., Nie H., Hong Y., Sheng C., Wang Q., Xia W., Ying W. NAD+ metabolism and NAD(+)-dependent enzymes: promising therapeutic targets for neurological diseases. Curr. Drug. Targets. 2012; 13 (2): 222–229.
  27. Salmina A.B., Olovyannikova R.Ya., M. Noda, and Higashida H. NAD+ metabolism and ADP-ribosyl cyclase as targets for central nervous system therapy. Curr. Medicin. Chem. 2006; 6: 193–210.
  28. Aksoy P., White T., Thompson M. Regulation of intracellular levels of NAD+: a novel role for CD38. Biochem. Biophys. Res. Commun. 2006; 10: 1016.
  29. Chini E.N. CD38 as a regulator of cellular NAD+: a novel potential pharmacological target for metabolic conditions. Curr. Pharm. Des. 2009; 15 (1): 57–63.
  30. Outeiro T.F., Marques O., Kazantsev A. Therapeutic role of sirtuins in neurodegenerative disease. Biochim. Biophys. Acta. 2008; 1782: 363–369.
  31. Tang B.L., Chua C.E.L. SIRT1 and neuronal diseases. Molecular Aspects of Medicine. 2008; 29: 187–200.
  32. Cohem D.E., Supinski A.M., Bonkowski M.S., Donmez G., Guarente L.P. Neuronal SIRT1 regulates endocrine and behavioral responses to calorie restriction. Genes & Development. 2009; 23: 2812–2817.
  33. Michan S., Li Y., Chou M .M-H., Parrella E., Ge H., Long J.M., Allard J.S., Lewis K., Miller M., Xu W., Mervis R.F., Chen J., Guerin K.I., Smith L.E., McBurney M.W., Sinclair D.A., Baudry M., de Cabo R., Longo V.D. SIRT1 is essential for normal cognitive function and synaptic plasticity. J. Neurosci. 2010; 30 (29): 9695–9707.
  34. Aksoy P., Escande C, White T.A., Thompson M., Soares S., Benech J.C., Chini E.N. Regulation of SIRT 1 mediated NAD dependent deacetylation: a novel role for the multifunctional enzyme CD38. Biochem. Biophys. Res. Commun. 2006; 349: 353–359.
  35. Sahar S., Nin V., Barbosa M.T., Chini E.N., Sassone-Corsi P. Altered behavioral and metabolic circadian rhythms in mice with disrupted NAD+ oscillation. Aging. 2011; 3 (8): 1–9.
  36. Wang S.H., Liao X.M., Liu D., Hu J., Yin Y.Y., Wang J.Z., Zhu L.Q. NGF promotes long-term memory formation by activating poly(ADP-ribose)polymerase-1. Neuropharmacology. 2012; 63 (6): 1085–1092.
  37. Morikawa H., Khodakhah K., Williams J.T. Two intracellular pathways mediate metabotropic glutamate receptor-induced Ca2+ mobilization in dopamine neurons. J. Neurosci. 2003; 23 (1): 149–157.
  38. Matyash M., Matyash V., Nolte C., Sorrentino V., Kettenmann H. Requirement of functional ryanodine receptor type 3 for astrocyte migration. FASEB J. 2002; 16 (1): 84–86.
  39. Simpson P.B., Holtzclaw L.A., Langley D.B., Russell J.T. Characterization of ryanodine receptors in oligodendrocytes, type 2 astrocytes, and O-2A progenitors. J. Neurosci. Res. 1998; 52 (4): 468–482.
  40. Chung K.K., Freestone P.S., Lipski J. Expression and functional properties of TRPM2 channels in dopaminergic neurons of the substantia nigra of the rat. J. Neurophysiol. 2011; 106 (6): 2865–2875.
  41. Toth B., and Csanady L. Identification of direct and indirect effectors of the transient receptor potential melastatin 2 (TRPM2) cation channel. J .Biol. Chem. 2010; 285 (39): 30091–30102.
  42. Massullo P., Sumoza-Toledo A., Bhagat H., Partida-Sánchez S. TRPM channels, calcium and redox sensors during innate immune responses. Seminars in Cell & Developmental Biol. 2006; 17: 654–666.
  43. Nazıroglu M. TRPM2 cation channels, oxidative stress and neurological diseases: where are we now? Neurochem. Res. 2011; 36 (3): 355–366.
  44. Lu H., Burns D., Garnier P., Wei G., Zhu K., Ying W. P2X7 receptors mediate NADH transport across the plasma membrane of astrocytes. Biochem. Biophys. Res. Comm. 2007; 362: 946–950.
  45. Bruzzone S., Basile G., Chothi M.P., Nobbio L., Usai C., Jacchetti E., Schenone A., Guse A.H., Di Virgilio F., De Flora A., Zocchi E. Diadenosine homodinucleotide products of ADP-ribosyl cyclase behave as modulators of the purinergic receptor P2X7. J. Biol. Chem. 2010; 285 (27): 21165–21174.
  46. Malavasi F., Deaglio S., Zaccarello G., Horenstein A.L., Chillemi A., Audrito V., Serra S., Gandione M., Zitella A., Tizzani A. The hidden life of NAD+-consuming ectoenzymes in the endocrine system. J. Mol. Endocrinol. 2010; 45: 183–191.
  47. Fields R.D., Burnstock G. Purinergic signaling in neuron-glia interactions. Nature Rev. Neurosci. 2006; 7: 423–436
  48. Wilhelm F., Hirrlinger J. Multifunctional roles of NAD+ and NADH in astrocytes. Neurochem. Res. 2012; doi: 10.1007/s11064-012-0760-y.
  49. Bambrick L., Kristian T., Fiskum G. Astrocyte mitochondrial mechanisms of ischemic brain injury and neuroprotection. Neurochemical Res. 2004; 29 (3): 601–608.
  50. Jacobson J., Duchen M.R. Mitochondrial oxidative stress and cell death in astrocytes - requirement for stored Ca2+ and sustained opening of the permeability transition pore. J. Cell Sci. 2002; 115: 1175–1188.
  51. Sonnewald U., Qu H., Ascher M. Pharmacology and toxicology of astrocyte-neuron glutamate transport and cycling. J. Pharmacol. Exp. Therap. 2002; 301: 1–6.
  52. Bruzzone S., Dodoni G., Kaludercic N., Basile G., Millo E., De Flora A., Di Lisa F., Zocchi E. Mitochondrial dysfunction induced by a cytotoxic adenine dinucleotide produced by ADP-ribosyl cyclases from cADPR. J. Biol. Chem. 2007; 282 (7): 5045–5052.
  53. Haydon P.G., Carmignoto G. Astrocyte control of synaptic transmission and neurovascular coupling. Physiol. Rev. 2006; 86: 1009–1031.
  54. Nakase T., Söhl G., Theis M., Willecke K., Naus C.C. Increased apoptosis and inflammation after focal brain ischemia in mice lacking connexin 43 in astrocytes. Am. J. Pathol. 2004; 164: 2067–2075.
  55. De Pina-Benabou M.H., Szostak V., Kyrozis A., Rempe D., Uziel D., Urban-Maldonado M., Benabou S., Spray D.C., Federoff H.J., Stanton P.K., Rozental R. Blockade of gap junctions in vivo provides neuroprotection after perinatal global ischemia. Stroke. 2005; 36: 2232–2237.
  56. De Flora A., Zocchi E., Guida L., Franco L., Bruzzone S. Autocrine and paracrine calcium signaling by the CD38/NAD+/cyclic ADP-ribose system. Ann. NY Acad. Sci. 2006; 1028: 176–191.
  57. Contreras J.E., Sánchez H.A., Eugenin E.A., Speidel D., Theis M., Willecke K., Bukauskas F.F., Bennett M.V., Sáez J.C. Metabolic inhibition induces opening of unapposed connexin 43 gap junction hemichannels and reduces gap junctional communication in cortical astrocytes in culture. Proc. Natl. Acad. Sci. 2001; 10: 1073.
  58. Bruzzone S., Verderio C., Schenk U., Fedele E., Zocchi E., Matteoli M., De Flora A. Glutamate-mediated overexpression of CD38 in astrocytes cultured with neurons. J. Neurochem. 2004; 89: 264.
  59. Winship I.R., Plaa N., and Murphy T.H. Rapid astrocyte calcium signals correlate with neuronal activity and onset of the hemodynamic response in vivo. J. Neurosci. 2007; 27: 6268–6272.
  60. Alano C.C., Ying W., Swanson R.A. Poly(ADP-ribose)polymerase-1-mediated cell death in astrocytes requires NAD+ depletion and mitochondrial permeability transition. J. Biol. Chem. 2004; 279: 18895–18902.
  61. Salmina A.B., Fursov A.A., Mikhutkina S.V., Malinovskaya N.A., Morgun A.V., Zykova L.D., Musaeva O.F., Fursov M.A., Laletin D.I., Yudin G.V., Trufanova L.V., Shnaider N.A. Progression of apoptosis and alteration in ADP-ribosyl cyclase activity in ischemic brain injury. Sibirskoe meditsinskoe obozrenie = Siberian medical review. 2006; 4: 22–27.
  62. Salmina A.B., Malinovskaya N.A., Okuneva O.S., Taranushenko T.E., Fursov A.A., Mihutkina S.V., Morgun A.V., Prokopenko S.V., Zikova L.D. Perinatal hypoxic-ischemic central nervous system damage induces alterations in expression of Cx43, CD38 and activity of ADP-ribosyl cyclase in brain cells. Bull. Exp. Biol. Med., 2008; 146 (12): 641–645.
  63. Salmina A.B., Okuneva O.S., Malinovskaya N.A., Zykova L.D., Fursov A.A., Morgun A.V., Mihutkina S.V., Taranushenko T.E. Changes in expression and activity of CD38 in astroglial cells after impairment of the neuron-glia relationship in the brain induced by perinatal hypoxia ischemia. J. Neurochem. 2009; 3 (3): 207–213.
  64. Mayo L., Jacob-Hirsch J., Amariglio N., Rechavi G., Moutin M.J., Lund F.E., Stein R. Dual role of CD38 in microglial activation and activation induced cell death. J. Immunol. 2008; 181: 92–103.
  65. Williams A.C., Cartwright L.S., Ramsden D.B. Parkinson’s disease: the first common neurological disease due to auto-intoxication. Q.J. Med., 2005; 98: 215–226.
  66. Levy A., Bercovich-Kinori A., Alexandrovich A.G., Tsenter J., Trembovler V., Lund F.E., Shohami E., Stein R., Mayo L. CD38 facilitates recovery from traumatic brain injury. J. Neurotrauma. 2009; 26: 1521–1533.
  67. Miller C.L. The evolution of schizophrenia: a model for selection by infection, with a focus on NAD. Curr. Pharmacol. Des., 2009; 15: 100–109.
  68. Salmina A.B., Lopatina O., Ekimova M.V., Mikhutkina S.V., Higashida H. CD38/Cyclic ADP-ribose System: A new player for oxytocin secretion and regulation of social behaviour. J. Neuroendocrinology. 2010; 22 (5): 380–392.
  69. Khan J.A., Forouhar F., Tao X., Tong L. Nicotinamide adenine dinucleotide metabolism as an attractive target for drug discovery. Expert Opin. Ther. Targets. 2007; 11 (5): 695–705.
  70. Ebstein R.P., Mankuta D., Yirmiya N., Malavasi F. Are retinoids potential therapeutic agents in disorders of social cognition including autism? FEBS Lett. 2011; 585 (11):1529–1536.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2012 "Paediatrician" Publishers LLC



This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies