A cytoprotective role for the heme oxygenase-1/CO pathway during neural differentiation of human mesenchymal stem cells

Journal of Neuroscience Research

Volumn 86, Issue 9, 2008, Pages 1927-1935

  Barbagallo, Ignazio ^a,b   Tibullo, Daniele ^b   Di Rosa, Michelino ^b   Giallongo, Cesarina ^b   Palumbo, Giuseppe A ^b   Raciti, Giuseppina ^b   Campisi, Agata ^b   Vanella, Angelo ^b   Green, Colin J ^a   Motterlini, Roberto ^a  

^a NORTHWICK PARK INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b UNIVERSITY OF CATANIA   (Italy)

Author keywords

Carbon monoxide; Cytoprotection; Glutamate toxicity; Heme oxygenase 1; Neural differentiation; Stem cells

Indexed keywords

BILIVERDIN; CARBON MONOXIDE; GLUTAMIC ACID; HEME OXYGENASE 1; HEMIN; LACTATE DEHYDROGENASE; MESSENGER RNA;

ARTICLE; CATALYSIS; CATALYST; CELL DAMAGE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; ENZYME RELEASE; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; NERVE CELL DIFFERENTIATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION;

BONE MARROW CELLS; CARBON MONOXIDE; CELL DIFFERENTIATION; CULTURE MEDIA; CYTOPROTECTION; DNA PRIMERS; HEME OXYGENASE-1; HUMANS; L-LACTATE DEHYDROGENASE; MESENCHYMAL STEM CELLS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 48249113786     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.21660     Document Type: Article

References (34)

1. Bani-Hani MG, Greenstein D, Mann BE, Green CJ, Motterlini R. 2006. A carbon monoxide - releasing molecule (CORM-3) attenuates lipopolysaccharide- and interferon-gamma-induced inflammation in microglia. Pharmacol Rep 58(Suppl):132-144.
2. Blondheim NR, Levy YS, Ben Zur T, Burshtein A, Cherlow T, Kan I, Barzilai R, Bahat-Stromza M, Barhum Y, Bulvik S, Melamed E, Offen D. 2006. Human mesenchymal stem cells express neural genes, suggesting a neural predisposition. Stem Cells Dev 15:141-164.
3. Boczkowski J, Poderoso JJ, Motterlini R. 2006. CO-metal interaction: vital signaling from a lethal gas. Trends Biochem Sci 31:614-621.
4. Clark JE, Foresti R, Sarathchandra P, Kaur H, Green CJ, Motterlini R. 2000. Heme oxygenase-1-derived bilirubin ameliorates post-ischemic myocardial dysfunction. Am J Physiol Heart Circ Physiol 278:H643-H651.
5. Clark JE, Naughton P, Shurey S, Green CJ, Johnson TR, Mann BE, Foresti R, Motterlini R. 2003. Cardioprotective actions by a water-soluble carbon monoxide-releasing molecule. Circ Res 93:e2-e8.
6. Deng J, Petersen BE, Steindler DA, Jorgensen ML, Laywell ED. 2006a. Mesenchymal stem cells spontaneously express neural proteins in culture and are neurogenic after transplantation. Stem Cells 24:1054-1064.
7. Deng YB, Liu XG, Liu ZG, Liu XL, Liu Y, Zhou GQ. 2006b. Implantation of BM mesenchymal stem cells into injured spinal cord elicits de novo neurogenesis and functional recovery: evidence from a study in rhesus monkeys. Cytotherapy 8:210-214.
8. Ferrari G, Cusella-De Angelis G, Coletta M, Paolucci E, Stornaiuolo A, Cossu G, Mavilio F. 1998. Muscle regeneration by bone marrow-derived myogenic progenitors. Science 279:1528-1530.
9. Foresti R, Clark JE, Green CJ, Motterlini R. 1997. Thiol compounds interact with nitric oxide in regulating heme oxygenase-1 induction in endothelial cells. Involvement of superoxide and peroxynitrite anions. J Biol Chem 272:18411-18417.
10. Foresti R, Motterlini R. 1999. The heme oxygenase pathway and its interaction with nitric oxide in the control of cellular homeostasis. Free Radic Res 31:459-475.
11. Foresti R, Green CJ, Motterlini R. 2004. Generation of bile pigments by heme oxygenase: a refined cellular stratagem in response to stressful insults. Biochem Soc Symp 71:177-192.
12. Ishii DN, Maniatis GM. 1978. Haemin promotes rapid neurite outgrowth in cultured mouse neuroblastoma cells. Nature 274:372-374.
13. Johnson TR, Mann BE, Teasdale IP, Adams H, Foresti R, Green CJ, Motterlini R. 2007. Metal carbonyls as pharmaceuticals? [Ru(CO)(3)Cl(glycinate)] , a CO-releasing molecule with an extensive aqueous solution chemistry. Dalton Trans1500-1508.
14. Kim HP, Ryter SW, Choi AM. 2006. CO as a cellular signaling molecule. Annu Rev Pharmacol Toxicol 46:411-449.
15. Li Volti G, Ientile R, Abraham NG, Vanella A, Cannavo G, Mazza F, Curro M, Raciti G, Avola R, Campisi A. 2004. Immunocytochemical localization and expression of heme oxygenase-1 in primary astroglial cell cultures during differentiation: effect of glutamate. Biochem Biophys Res Commun 315:517-524.
16. Long X, Olszewski M, Huang W, Kletzel M. 2005. Neural cell differentiation in vitro from adult human bone marrow mesenchymal stem cells. Stem Cells Dev 14:65-69.
17. Madhavan L, Ourednik V, Ourednik J. 2005. Grafted neural stem cells shield the host environment from oxidative stress. Ann N Y Acad Sci 1049:185-188.
18. Maines MD. 1997. The heme oxygenase system: a regulator of second messenger gases. Annu Rev Pharmacol Toxicol 37:517-554.
19. Motterlini R, Foresti R, Intaglietta M, Winslow RM. 1996. NO-mediated activation of heme oxygenase: endogenous cytoprotection against oxidative stress to endothelium. Am J Physiol Heart Circ Physiol 270:H107-H114.
20. Motterlini R, Gonzales A, Foresti R, Clark JE, Green CJ, Winslow RM. 1998. Heme oxygenase-1-derived carbon monoxide contributes to the suppression of acute hypertensive responses in vivo. Circ Res 83:568-577.
21. Motterlini R, Mann BE, Johnson TR, Clark JE, Foresti R, Green CJ. 2003. Bioactivity and pharmacological actions of carbon monoxide-releasing molecules. Curr Pharmacol Design 9:2525-2539.
22. Motterlini R, Mann BE, Foresti R. 2005a. Therapeutic applications of carbon monoxide-releasing molecules (CO-RMs). Expert Opin Investig Drugs 14:1305-1318.
23. Motterlini R, Sawle P, Bains S, Hammad J, Alberto R, Foresti R, Green CJ. 2005b. CORM-A1: a new pharmacologically active carbon monoxide-releasing molecule. FASEB J 19:284-286.
24. Otterbein LE, Bach FH, Alam J, Soares M, Tao Lu H, Wysk M, Davis RJ, Flavell RA, Choi AM. 2000. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 6:422-428.
25. Otterbein LE, Soares MP, Yamashita K, Bach FH. 2003. Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol 24:449-455.
26. Parfenova H, Basuroy S, Bhattacharya S, Tcheranova D, Qu Y, Regan RF, Leffler CW. 2005. Glutamate induces oxidative stress and apoptosis in cerebral vascular endothelial cells: contributions of HO-1 and HO-2 to cytoprotection. Am J Physiol Cell Physiol 290:C1399-C1410.
27. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. 1999. Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147.
28. Qu Y, Vadivelu S, Choi L, Liu S, Lu A, Lewis B, Girgis R, Lee CS, Snider BJ, Gottlieb DI, McDonald JW. 2003. Neurons derived from embryonic stem (ES) cells resemble normal neurons in their vulnerability to excitotoxic death. Exp Neurol 184:326-336.
29. Sandouka A, Fuller BJ, Mann BE, Green CJ, Foresti R, Motterlini R. 2006. Treatment with carbon monoxide-releasing molecules (CO-RMs) during cold storage improves renal function at reperfusion. Kidney Int 69:239-247.
30. Suzuki H, Taguchi T, Tanaka H, Kataoka H, Li Z, Muramatsu K, Gondo T, Kawai S. 2004. Neurospheres induced from bone marrow stromal cells are multipotent for differentiation into neuron, astrocyte, and oligodendrocyte phenotypes. Biochem Biophys Res Commun 322:918-922.
31. Tayem Y, Johnson TR, Mann BE, Green CJ, Motterlini R. 2006. Protection against cisplatin-induced nephrotoxicity by a carbon monoxide-releasing molecule. Am J Physiol Renal Physiol 290:F789-F794.
32. Wislet-Gendebien S, Hans G, Leprince P, Rigo JM, Moonen G, Rogister B. 2005. Plasticity of cultured mesenchymal stem cells: switch from nestin-positive to excitable neuron-like phenotype. Stem Cells 23:392-402.
33. Zhao LR, Duan WM, Reyes M, Keene CD, Verfaillie CM, Low WC. 2002. Human bone marrow stem cells exhibit neural phenotypes and ameliorate neurological deficits after grafting into the ischemic brain of rats. Exp Neurol 174:11-20.
34. Zhou H, Ramiya VK, Visner GA. 2006. Bone marrow stem cells as a vehicle for delivery of heme oxygenase-1 gene. Stem Cells Dev 15:79-86.