Heparin-binding epidermal growth factor-like growth factor: Hypoxia-inducible expression in vitro and stimulation of neurogenesis in vitro and in vivo

Journal of Neuroscience

Volumn 22, Issue 13, 2002, Pages 5365-5373

  Jin, Kunlin ^a   Ou Mao, Xiao ^a   Sun, Yunjuan ^a   Xie, Lin ^a   Jin, Lan ^a   Nishi, Eiichiro ^b   Klagsbrun, Michael ^b   Greenberg, David A ^a  

^a BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Epidermal growth factor receptor (EGFR ErbB1); Heparin binding epidermal growth factor like growth factor (HB EGF); Hypoxia; Ischemia; N arginine dibasic convertase (NRDc); Neurogenesis

Indexed keywords

BROXURIDINE; EPIDERMAL GROWTH FACTOR RECEPTOR; GROWTH FACTOR RECEPTOR; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; METALLOPROTEINASE; N ARGININE DIBASIC CONVERTASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN HYPOXIA; CELL CULTURE; CELL LABELING; CELL MATURATION; CELL PROLIFERATION; DENTATE GYRUS; EMBRYO; MALE; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION;

EID: 0036662775     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-13-05365.2002     Document Type: Article

References (44)

1. Brewer GJ, Torricelli JR, Evege EK, Price PJ (1993) Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J Neurosci Res 35:567-576.
2. Chen J, Jin K, Chen M, Pei W, Kawaguchi K, Greenberg DA, Simon RP (1997) Early detection of DNA strand breaks in the brain after transient focal ischemia: Implications for the role of DNA damage in apoptosis and neuronal cell death. J Neurochem 69:232-245.
3. Cramer SC, Chopp M (2000) Recovery recapitulates ontogeny. Trends Neurosci 23:265-271.
4. Davis-Fleischer KM, Besner GE (1998) Structure and function of heparin-binding EGF-like growth factor (HB-EGF). Front Biosci 3:288-299.
5. Dong J, Wiley HS (2000) Trafficking and proteolytic release of epidermal growth factor receptor ligands are modulated by their membraneanchoring domains. J Biol Chem 275:557-564.
6. Fujita M, Kiyono T, Hayashi Y, Ishibashi M (1996) hCDC47, a human member of the MCM family. Dissociation of the nucleus-bound form during S phase. J Biol Chem 271:4349-4354.
7. Gechtman Z, Alonso JL, Raab G, Ingber DE, Klagsbrun M (1999) The shedding of membrane-anchored heparin-binding epidermal-like growth factor is regulated by the Raf/mitogen-activated protein kinase cascade and by cell adhesion and spreading. J Biol Chem 274:28828-28835.
8. Goldberg MP, Choi DW (1993) Combined oxygen and glucose deprivation in cortical cell culture: Calcium-dependent and calciumindependent mechanisms of neuronal injury. J Neurosci 13:3510-3524.
9. Gould E, Tanapat P (1997) Lesion-induced proliferation of neuronal progenitors in the dentate gyrus of the adult rat. Neuroscience 80:427-436.
10. Gu W, Brannstrom T, Wester P (2000) Cortical neurogenesis in adult rats after reversible photothrombotic stroke. J Cereb Blood Flow Metab 20:1166-1173.
11. Hayase Y, Higashiyama S, Sasahara M, Amano S, Nakagawa T, Taniguchi N, Hazama F (1998) Expression of heparin-binding epidermal growth factor-like growth factor in rat brain. Brain Res 784:163-178.
12. Hendzel MJ, Wei Y, Mancini MA, Van Hooser A, Ranalli T, Brinkley BR, Bazett-Jones DP, Allis CD (1997) Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106:348-360.
13. Higashiyama S, Abraham JA, Miller JA, Fiddes JC, Klagsbrun M (1991) A heparin-binding growth factor secreted by macrophage-like cells that is related to EGF. Science 251:936-939.
14. Ino H, Chiba T (2000) Expression of proliferating cell nuclear antigen (PCNA) in the adult and developing mouse nervous system. Brain Res Mol Brain Res 78:163-174.
15. Jiang W Gu W, Brännström T, Rosqvist R, Wester P (2001) Cortical neurogenesis in adult rats after transient middle cerebral artery occlusion. Stroke 32:1201-1207.
16. Jin K, Chen J, Nagayama T, Chen M, Sinclair J, Graham SH, Simon RP (1999) In situ detection of neuronal DNA strand breaks using the Klenow fragment of DNA polymerase I reveals different mechanisms of neuron death after global cerebral ischemia. J Neurochem 72:1204-1214.
17. Jin K, Minami M, Lan JQ, Mao XO, Batteur S, Simon RP, Greenberg DA (2001) Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc Natl Acad Sci USA 98:4710-4715.
18. Jost M, Kari C, Rodeck U (2000) The EGF receptor - An essential regulator of multiple epidermal functions. Eur J Dermatol 10:505-510.
19. Kawahara N, Mishima K, Higashiyama S, Taniguchi N, Tamura A, Kirino T (1999) The gene for heparin-binding epidermal growth factor-like growth factor is stress-inducible: Its role in cerebral ischemia. J Cereb Blood Flow Metab 19:307-320.
20. Koretz B, Ahern KB, Lustig HS, Greenberg DA (1994) Pre- and postsynaptic modulators of excitatory neurotransmission: Comparative effects on hypoxia/hypoglycemia in cortical cultures. Brain Res 643:334-337.
21. Krupinski J, Vodovotz Y LiC, Slowik A, Beevers D, Flanders KC, Lip G, Kumar P, Szczudlik A (1998) Inducible nitric oxide production and expression of transforming growth factor-betal in serum and CSF after cerebral ischaemic stroke in man. Nitric Oxide 2:442-453.
22. Kuhn HG, Winkler J, Kempermann G, Thal LJ, Gage FH (1997) Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J Neurosci 17:5820-5829.
23. Law RE, Meehan WP, Xi XP, Graf K, Wuthrich DA, Coats W, Faxon D, Hsueh WA (1996) Troglitazone inhibits vascular smooth muscle cell growth and intimal hyperplasia. J Clin Invest 98:1897-1905.
24. Lee JK, Cho JH, Hwang WS, Lee YD, Reu DS, Suh-Kim H (2000) Expression of neuroD/BETA2 in mitotic and postmitotic neuronal cells during the development of nervous system. Dev Dyn 217:361-367.
25. Lin J, Hutchinson L, Gaston SM, Raab G, Freeman MR (2001a) BAG-1 is a novel cytoplasmic binding partner of the membrane form of heparin-binding EGF-like growth factor: A unique role for proHB-EGF in cell survival regulation. J Biol Chem 276:30127-30132.
26. Lin SY, Makino K, Xia W, Matin A, Wen Y, Kwong KY, Bourguignon L, Hung MC (2001b) Nuclear localization of EGF receptor and its potential new role as a transcription factor. Nat Cell Biol 3:802-808.
27. Liu J, Solway K, Messing RO, Sharp FR (1998) Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils. J Neurosci 18:7768-7778.
28. Magavi SS, Leavitt BR, Macklis JD (2000) Induction of neurogenesis in the neocortex of adult mice. Nature 405:951-955.
29. Mishima K, Higashiyama S, Nagashima Y, Miyagi Y, Tamura A, Kawahara N, Taniguchi N, Asai A, Kuchino Y, Kirino T (1996) Regional distribution of heparin-binding epidermal growth factor-like growth factor mRNA and protein in adult rat forebrain. Neurosci Lett 213:153-156.
30. Naglich JG, Metherall JE, Russell DW, Eidels L (1992) Expression cloning of a diphtheria toxin receptor: Identity with a heparin-binding EGF-like growth factor precursor. Cell 69:1051-1061.
31. Nakagawa T, Sasahara M, Hayase Y, Haneda M, Yasuda H, Kikkawa R, Higashiyama S, Hazama F (1998) Neuronal and glial expression of heparin-binding EGF-like growth factor in central nervous system of prenatal and early-postnatal rat. Brain Res Dev Brain Res 108:263-272.
32. Nishi E, Prat A, Hospital V, Elenius K, Klagsbrun M (2001) N-arginine dibasic convertase is a specific receptor for heparin-binding EGF-like growth factor that mediates cell migration. EMBO J 20:3342-3350.
33. Opanashuk LA, Hauser KF (1998) Opposing actions of the EGF family and opioids: Heparin binding-epidermal growth factor (HB-EGF) protects mouse cerebellar neuroblasts against the antiproliferative effect of morphine. Brain Res 804:87-94.
34. Opanashuk LA, Mark RJ, Porter J, Damm D, Mattson MP, Seroogy KB (1999) Heparin-binding epidermal growth factor-like growth factor in hippocampus: Modulation of expression by seizures and anti-excitotoxic action. J Neurosci 19:133-146.
35. Parent JM, Yu TW, Leibowitz RT, Geschwind DH, Sloviter RS, Lowenstein DH (1997) Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 17:3727-3738.
36. Pencea V, Bingaman KD, Wiegand SJ, Luskin MB (2001) Infusion of brain-derived neurotrophic factor into the lateral ventricle of the adult rat leads to new neurons in the parenchyma of the striatum, septum, thalamus, and hypothalamus. J Neurosci 21:6706-6717.
37. Raab G, Klagsbrun M (1997) Heparin-binding EGF-like growth factor. Biochim Biophys Acta 1333:F179-199.
38. Reynolds BA, Tetzlaff W, Weiss S (1992) A multipotent EGF-responsive striatal embyronic progenitor cell produces neurons and astrocytes. J Neurosci 12:4565-4574.
39. Sun Y, Jin K, Mao XO, Zhu Y, Greenberg DA (2001) Neuroglobin is upregulated by and protects neurons from hypoxic-ischemic injury. Proc Natl Acad Sci USA 98:15306-15311.
40. Takagi Y, Nozaki K, Takahashi J, Yodoi J, Ishikawa M, Hashimoto N (1999) Proliferation of neuronal precursor cells in the dentate gyrus is accelerated after transient forebrain ischemia in mice. Brain Res 831:283-287.
41. Tanaka N, Sasahara M, Ohno M, Higashiyama S, Hayase Y, Shimada M (1999) Heparin-binding epidermal growth factor-like growth factor mRNA expression in neonatal rat brain with hypoxic/ischemic injury. Brain Res 827:130-138.
42. Yoshimura S, Takagi Y, Harada J, Teramoto T, Thomas SS, Waeber C, Bakowska JC, Breakefield XO, Moskowitz MA (2001) FGF-2 regulation of neurogenesis in adult hippocampus after brain injury. Proc Natl Acad Sci USA 98:5874-5879.
43. Zhang RL, Zhang ZG, Zhang L, Chopp M (2001) Proliferation and differentiation of progenitor cells in the cortex and the subventricular zone in the adult rat after focal cerebral ischemia. Neuroscience 105:33-41.
44. Zigova T, Pencea V, Wiegand SJ, Luskin MB (1998) Intraventricular administration of BDNF increases the number of newly generated neurons in the adult olfactory bulb. Mol Cell Neurosci 11:234-245.