Hyperforin promotes mitochondrial function and development of oligodendrocytes

Journal of Neurochemistry

Volumn 119, Issue 3, 2011, Pages 555-568

  Wang, Yanlin ^a   Zhang, Yanbo ^a,b   He, Jue ^b   Zhang, Handi ^b   Xiao, Lan ^c   Nazarali, Adil ^d   Zhang, Zhijun ^e   Zhang, Dai ^f   Tan, Qingrong ^g   Kong, Jiming ^h   Li, Xin Min ^a,b,h  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b UNIVERSITY OF MANITOBA   (Canada)

^c THIRD MILITARY MEDICAL UNIVERSITY   (China)

^d UNIVERSITY OF SASKATCHEWAN   (Canada)

^e SOUTHEAST UNIVERSITY   (China)

^f PEKING UNIVERSITY SIXTH HOSPITAL   (China)

^g FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^h UNIVERSITY OF MANITOBA   (Canada)

Author keywords

development; hyperforin; mitochondrial function; oligodendrocyte; St. John's wort

Indexed keywords

HYPERFORIN; TOXIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXICITY; DEPRESSION; DRUG EFFECT; FETUS; HYPERICUM PERFORATUM; MITOCHONDRION; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; RAT;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; CELLS, CULTURED; MITOCHONDRIA; OLIGODENDROGLIA; PHLOROGLUCINOL; RATS; STEM CELLS; TERPENES;

EID: 80054052110     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2011.07433.x     Document Type: Article

References (77)

1. Aston C., Jiang L., and, Sokolov B. P., (2005) Transcriptional profiling reveals evidence for signaling and oligodendroglial abnormalities in the temporal cortex from patients with major depressive disorder. Mol. Psychiatry 10, 309-322. (Pubitemid 40432684)
2. Benes F. M., Turtle M., Khan Y., and, Farol P., (1994) Myelination of a key relay zone in the hippocampal formation occurs in the human brain during childhood, adolescence, and adulthood. Arch. Gen. Psychiatry 51, 477-484. (Pubitemid 24180494)
3. Bergles D. E., Roberts J. D., Somogyi P., and, Jahr C. E., (2000) Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus. Nature 405, 187-191. (Pubitemid 30313537)
4. Bernardo A., Bianchi D., Magnaghi V., and, Minghetti L., (2009) Peroxisome proliferator-activated receptor-gamma agonists promote differentiation and antioxidant defenses of oligodendrocyte progenitor cells. J. Neuropathol. Exp. Neurol. 68, 797-808.
5. Berridge M. V., Herst P. M., and, Tan A. S., (2005) Tetrazolium dyes as tools in cell biology: new insights into their cellular reduction. Biotechnol. Annu. Rev. 11, 127-152. (Pubitemid 41510276)
6. Berton O., and, Nestler E. J., (2006) New approaches to antidepressant drug discovery: beyond monoamines. Nat. Rev. Neurosci. 7, 137-151. (Pubitemid 43151600)
7. Boyer P. D., Chance B., Ernster L., Mitchell P., Racker E., and, Slater E. C., (1977) Oxidative phosphorylation and photophosphorylation. Annu. Rev. Biochem. 46, 955-966.
8. 18F]2-deoxyglucose in affective illness. J. Affect. Disord. 10, 137-152. (Pubitemid 16067656)
9. Burigo M., Roza C. A., Bassani C., Fagundes D. A., Rezin G. T., Feier G., Dal-Pizzol F., Quevedo J., and, Streck E. L., (2006) Effect of electroconvulsive shock on mitochondrial respiratory chain in rat brain. Neurochem. Res. 31, 1375-1379. (Pubitemid 44800589)
10. Cabrelle A., Dell'Aica I., and, Melchiori L., et al. (2008) Hyperforin down-regulates effector function of activated T lymphocytes and shows efficacy against Th1-triggered CNS inflammatory-demyelinating disease. J. Leukoc. Biol. 83, 212-219.
11. Cai J., Chen Y., Cai W. H., Hurlock E. C., Wu H., Kernie S. G., Parada L. F., and, Lu Q. R., (2007) A crucial role for Olig2 in white matter astrocyte development. Development 134, 1887-1899. (Pubitemid 46939234)
12. Cervo L., Rozio M., Ekalle-Soppo C. B., Guiso G., Morazzoni P., and, Caccia S., (2002) Role of hyperforin in the antidepressant-like activity of Hypericum perforatum extracts. Psychopharmacology (Berl) 164, 423-428. (Pubitemid 35439171)
13. 11C]methoxy)rotenone, a marker of mitochondrial complex I activity. Nucl. Med. Biol. 22, 65-69.
14. Chen L. B., Summerhayes I. C., Johnson L. V., Walsh M. L., Bernal S. D., and, Lampidis T. J., (1982) Probing mitochondria in living cells with rhodamine 123. Cold Spring Harb. Symp. Quant. Biol. 46 (Pt 1), 141-155.
15. Connor J. R., and, Menzies S. L., (1996) Relationship of iron to oligodendrocytes and myelination. Glia 17, 83-93. (Pubitemid 26309437)
16. Copray S., Balasubramaniyan V., Levenga J., de Bruijn J., Liem R., and, Boddeke E., (2006) Olig2 overexpression induces the in vitro differentiation of neural stem cells into mature oligodendrocytes. Stem Cells 24, 1001-1010. (Pubitemid 44464733)
17. Di Carlo G., Borrelli F., Ernst E., and, Izzo A. A., (2001) St John's wort: Prozac from the plant kingdom. Trends Pharmacol. Sci. 22, 292-297. (Pubitemid 32523912)
18. Dinamarca M. C., Cerpa W., Garrido J., Hancke J. L., and, Inestrosa N. C., (2006) Hyperforin prevents beta-amyloid neurotoxicity and spatial memory impairments by disaggregation of Alzheimer's amyloid-beta-deposits. Mol. Psychiatry 11, 1032-1048. (Pubitemid 44631646)
19. Drechsel D. A., and, Patel M., (2008) Role of reactive oxygen species in the neurotoxicity of environmental agents implicated in Parkinson's disease. Free Radic. Biol. Med. 44, 1873-1886.
20. Drevets W. C., Price J. L., Simpson J. R., Jr, Todd R. D., Reich T., Vannier M., and, Raichle M. E., (1997) Subgenual prefrontal cortex abnormalities in mood disorders. Nature 386, 824-827. (Pubitemid 27181254)
21. Estornell E., (2000) Mitochondrial complex I: new insights from inhibitor assays. Protoplasma 213, 11-17.
22. Fattal O., Budur K., Vaughan A. J., and, Franco K., (2006) Review of the literature on major mental disorders in adult patients with mitochondrial diseases. Psychosomatics 47, 1-7. (Pubitemid 43017115)
23. Fields R. D., (2005) Myelination: an overlooked mechanism of synaptic plasticity? Neuroscientist 11, 528-531. (Pubitemid 41611864)
24. Fukuda S., Kondo T., Takebayashi H., and, Taga T., (2004) Negative regulatory effect of an oligodendrocytic bHLH factor OLIG2 on the astrocytic differentiation pathway. Cell Death Differ. 11, 196-202. (Pubitemid 38159643)
25. Gambarana C., Tolu P. L., Masi F., Rinaldi M., Giachetti D., Morazzoni P., and, De Montis M. G., (2001) A study of the antidepressant activity of Hypericum perforatum on animal models. Pharmacopsychiatry 34 (Suppl. 1), S42-44.
26. Gervois P., Fruchart J. C., and, Staels B., (2007) Drug Insight: mechanisms of action and therapeutic applications for agonists of peroxisome proliferator-activated receptors. Nat. Clin. Pract. Endocrinol. Metab. 3, 145-156. (Pubitemid 46146967)
27. Gratzner H. G., (1982) Monoclonal antibody to 5-bromo- and 5-iododeoxyuridine: A new reagent for detection of DNA replication. Science 218, 474-475. (Pubitemid 12000901)
28. Gritti A., Parati E. A., and, Cova L., et al. (1996) Multipotential stem cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor. J. Neurosci. 16, 1091-1100.
29. Hamidi M., Drevets W. C., and, Price J. L., (2004) Glial reduction in amygdala in major depressive disorder is due to oligodendrocytes. Biol. Psychiatry 55, 563-569. (Pubitemid 38315029)
30. Heneka M. T., and, Landreth G. E., (2007) PPARs in the brain. Biochim. Biophys. Acta 1771, 1031-1045. (Pubitemid 47208548)
31. Honer W. G., Falkai P., Chen C., Arango V., Mann J. J., and, Dwork A. J., (1999) Synaptic and plasticity-associated proteins in anterior frontal cortex in severe mental illness. Neuroscience 91, 1247-1255. (Pubitemid 29234254)
32. Houseknecht K. L., Cole B. M., and, Steele P. J., (2002) Peroxisome proliferator-activated receptor gamma (PPARgamma) and its ligands: a review. Domest. Anim. Endocrinol. 22, 1-23. (Pubitemid 34438654)
33. Kato T., Inubushi T., and, Kato N., (1998) Magnetic resonance spectroscopy in affective disorders. J. Neuropsychiatr. Clin. Neurosci. 10, 133-147. (Pubitemid 28241361)
34. Kong E. K., Peng L., Chen Y., Yu A. C., and, Hertz L., (2002) Up-regulation of 5-HT2B receptor density and receptor-mediated glycogenolysis in mouse astrocytes by long-term fluoxetine administration. Neurochem. Res. 27, 113-120. (Pubitemid 34242437)
35. Kornack D. R., and, Rakic P., (2001) Cell proliferation without neurogenesis in adult primate neocortex. Science 294, 2127-2130. (Pubitemid 33150663)
36. Krusekopf S., and, Roots I., (2005) St. John's wort and its constituent hyperforin concordantly regulate expression of genes encoding enzymes involved in basic cellular pathways. Pharmacogenet. Genomics 15, 817-829. (Pubitemid 41531730)
37. Laakmann G., Schule C., Baghai T., and, Kieser M., (1998) St. John's wort in mild to moderate depression: the relevance of hyperforin for the clinical efficacy. Pharmacopsychiatry 31 (Suppl. 1), 54-59. (Pubitemid 28294226)
38. Laggner H., Schreier S., Hermann M., Exner M., Muhl A., Gmeiner B. M., and, Kapiotis S., (2007) The main components of St John's Wort inhibit low-density lipoprotein atherogenic modification: a beneficial "side effect" of an OTC antidepressant drug? Free Radic. Res. 41, 234-241. (Pubitemid 46992874)
39. Linde K., Berner M. M., and, Kriston L., (2008) St John's wort for major depression. Cochrane Database Syst. Rev. 4, CD000448.
40. Louis J. C., Magal E., Muir D., Manthorpe M., and, Varon S., (1992) CG-4, a new bipotential glial cell line from rat brain, is capable of differentiating in vitro into either mature oligodendrocytes or type-2 astrocytes. J. Neurosci. Res. 31, 193-204.
41. Lu Q. R., Yuk D., Alberta J. A., Zhu Z., Pawlitzky I., Chan J., McMahon A. P., Stiles C. D., and, Rowitch D. H., (2000) Sonic hedgehog-regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system. Neuron 25, 317-329.
42. Lu Q. R., Sun T., Zhu Z., Ma N., Garcia M., Stiles C. D., and, Rowitch D. H., (2002) Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell 109, 75-86. (Pubitemid 34327518)
43. Madsen T. M., Yeh D. D., Valentine G. W., and, Duman R. S., (2005) Electroconvulsive seizure treatment increases cell proliferation in rat frontal cortex. Neuropsychopharmacology 30, 27-34. (Pubitemid 40024396)
44. Magnus T., Coksaygan T., and, Korn T., et al. (2007) Evidence that nucleocytoplasmic Olig2 translocation mediates brain-injury-induced differentiation of glial precursors to astrocytes. J. Neurosci. Res. 85, 2126-2137. (Pubitemid 47172144)
45. McElroy W. D., and, DeLuca M. A., (1983) Firefly and bacterial luminescence: basic science and applications. J. Appl. Biochem. 5, 197-209.
46. McNulty S., Crouch M., Smart D., and, Rumsby M., (2001) Differentiation of bipolar CG-4 line oligodendrocytes is associated with regulation of CREB, MAP kinase and PKC signalling pathways. Neurosci. Res. 41, 217-226. (Pubitemid 32982889)
47. Muller W. E., Singer A., and, Wonnemann M., (2001) Hyperforin- antidepressant activity by a novel mechanism of action. Pharmacopsychiatry 34 (Suppl. 1), S98-102.
48. Neary J. T., Whittemore S. R., Bu Y., Mehta H., and, Shi Y. F., (2001) Biochemical mechanisms of action of Hypericum LI 160 in glial and neuronal cells: inhibition of neurotransmitter uptake and stimulation of extracellular signal regulated protein kinase. Pharmacopsychiatry 34 (Suppl. 1), S103-107.
49. Noble M., Wren D., and, Wolswijk G., (1992) The O-2A(adult) progenitor cell: a glial stem cell of the adult central nervous system. Semin. Cell Biol. 3, 413-422.
50. Noble M., Smith J., Power J., and, Mayer-Proschel M., (2003) Redox state as a central modulator of precursor cell function. Ann. N Y Acad. Sci. 991, 251-271. (Pubitemid 36793819)
51. Okuda H., Tatsumi K., Makinodan M., Yamauchi T., Kishimoto T., and, Wanaka A., (2009) Environmental enrichment stimulates progenitor cell proliferation in the amygdala. J. Neurosci. Res. 87, 3546-3553.
52. Pennington K., Focking M., McManus C., Pariante C., Dunn M., and, Cotter D., (2009) A proteomic investigation of similarities between conventional and herbal antidepressant treatments. J. Psychopharmacol. 23, 520-530.
53. Pleasure D., Abramsky O., Silberberg D., Quinn B., Parris J., and, Saida T., (1977) Lipid synthesis by an oligodendroglial fraction in suspension culture. Brain Res. 134, 377-382. (Pubitemid 8185504)
54. Qi Y., Cai J., and, Wu Y., et al. (2001) Control of oligodendrocyte differentiation by the Nkx2.2 homeodomain transcription factor. Development 128, 2723-2733. (Pubitemid 32701001)
55. Regenold W. T., Phatak P., Marano C. M., Gearhart L., Viens C. H., and, Hisley K. C., (2007) Myelin staining of deep white matter in the dorsolateral prefrontal cortex in schizophrenia, bipolar disorder, and unipolar major depression. Psychiatry Res. 151, 179-188. (Pubitemid 46829420)
56. Rezin G. T., Cardoso M. R., Goncalves C. L., Scaini G., Fraga D. B., Riegel R. E., Comim C. M., Quevedo J., and, Streck E. L., (2008) Inhibition of mitochondrial respiratory chain in brain of rats subjected to an experimental model of depression. Neurochem. Int. 53, 395-400.
57. Rosa A. O., Kaster M. P., and, Binfare R. W., et al. (2008) Antidepressant-like effect of the novel thiadiazolidinone NP031115 in mice. Prog. Neuropsychopharmacol. Biol. Psychiatry 32, 1549-1556.
58. Roth A. D., Leisewitz A. V., Jung J. E., Cassina P., Barbeito L., Inestrosa N. C., and, Bronfman M., (2003) PPAR gamma activators induce growth arrest and process extension in B12 oligodendrocyte-like cells and terminal differentiation of cultured oligodendrocytes. J. Neurosci. Res. 72, 425-435. (Pubitemid 36523417)
59. Rowitch D. H., Lu Q. R., Kessaris N., and, Richardson W. D., (2002) An 'oligarchy' rules neural development. Trends Neurosci. 25, 417-422. (Pubitemid 34804466)
60. Sanchez-Reus M. I., Gomez del Rio M. A., Iglesias I., Elorza M., Slowing K., and, Benedi J., (2007) Standardized Hypericum perforatum reduces oxidative stress and increases gene expression of antioxidant enzymes on rotenone-exposed rats. Neuropharmacology 52, 606-616. (Pubitemid 46123375)
61. Schempp C. M., Kirkin V., and, Simon-Haarhaus B., et al. (2002) Inhibition of tumour cell growth by hyperforin, a novel anticancer drug from St. John's wort that acts by induction of apoptosis. Oncogene 21, 1242-1250. (Pubitemid 34185241)
62. Sim F. J., Lang J. K., Ali T. A., Roy N. S., Vates G. E., Pilcher W. H., and, Goldman S. A., (2008) Statin treatment of adult human glial progenitors induces PPAR gamma-mediated oligodendrocytic differentiation. Glia 56, 954-962.
63. Singer A., Wonnemann M., and, Muller W. E., (1999) Hyperforin, a major antidepressant constituent of St. John's Wort, inhibits serotonin uptake by elevating free intracellular Na+1. J. Pharmacol. Exp. Ther. 290, 1363-1368. (Pubitemid 29400281)
64. Smith J., Ladi E., Mayer-Proschel M., and, Noble M., (2000) Redox state is a central modulator of the balance between self-renewal and differentiation in a dividing glial precursor cell. Proc. Natl. Acad. Sci. U S A 97, 10032-10037.
65. Sprinkle T. J., Zaruba M. E., and, McKhann G. M., (1978) Activity of 2′, 3′-cyclic-nucleotide 3′-phosphodiesterase in regions of rat brain during development: quantitative relationship to myelin basic protein. J. Neurochem. 30, 309-314. (Pubitemid 8283790)
66. Stanley P. E., (1986) Extraction of adenosine triphosphate from microbial and somatic cells. Methods Enzymol. 133, 14-22.
67. Stevens B., Tanner S., and, Fields R. D., (1998) Control of myelination by specific patterns of neural impulses. J. Neurosci. 18, 9303-9311. (Pubitemid 28512461)
68. Stolt C. C., Rehberg S., Ader M., Lommes P., Riethmacher D., Schachner M., Bartsch U., and, Wegner M., (2002) Terminal differentiation of myelin-forming oligodendrocytes depends on the transcription factor Sox10. Genes Dev. 16, 165-170. (Pubitemid 34075809)
69. 3H-valine incorporation and cell morphometry of astrocytes cultured from rat brain. Dev. Neurosci. 17, 292-299. (Pubitemid 26093255)
70. Uranova N. A., Vostrikov V. M., Orlovskaya D. D., and, Rachmanova V. I., (2004) Oligodendroglial density in the prefrontal cortex in schizophrenia and mood disorders: a study from the Stanley Neuropathology Consortium. Schizophr. Res. 67, 269-275. (Pubitemid 38251458)
71. Videbech P., (2000) PET measurements of brain glucose metabolism and blood flow in major depressive disorder: a critical review. Acta Psychiatr. Scand. 101, 11-20. (Pubitemid 30041119)
72. Wada K., Nakajima A., and, Katayama K., et al. (2006) Peroxisome proliferator-activated receptor gamma-mediated regulation of neural stem cell proliferation and differentiation. J. Biol. Chem. 281, 12673-12681. (Pubitemid 43855357)
73. Walczak R., and, Tontonoz P., (2002) PPARadigms and PPARadoxes: expanding roles for PPARgamma in the control of lipid metabolism. J. Lipid Res. 43, 177-186. (Pubitemid 34184004)
74. Wennstrom M., Hellsten J., and, Tingstrom A., (2004) Electroconvulsive seizures induce proliferation of NG2-expressing glial cells in adult rat amygdala. Biol. Psychiatry 55, 464-471. (Pubitemid 38338533)
75. Xiao L., Xu H., and, Zhang Y., et al. (2008) Quetiapine facilitates oligodendrocyte development and prevents mice from myelin breakdown and behavioral changes. Mol. Psychiatry 13, 697-708. (Pubitemid 351861531)
76. Xu X., Cai J., Fu H., Wu R., Qi Y., Modderman G., Liu R., and, Qiu M,. (2000) Selective expression of Nkx-2.2 transcription factor in chicken oligodendrocyte progenitors and implications for the embryonic origin of oligodendrocytes. Mol. Cell. Neurosci. 16, 740-753. (Pubitemid 32062061)
77. Zhou Q., Choi G., and, Anderson D. J,. (2001) The bHLH transcription factor Olig2 promotes oligodendrocyte differentiation in collaboration with Nkx2.2. Neuron 31, 791-807. (Pubitemid 32907374)