Hepatocyte growth factor protects retinal ganglion cells by increasing neuronal survival and axonal regeneration in vitro and in vivo

Journal of Neurochemistry

Volumn 117, Issue 5, 2011, Pages 892-903

  Tönges, Lars ^a   Ostendorf, Thomas ^a   Lamballe, Fabienne ^b   Genestine, Matthieu ^b   Dono, Rosanna ^b   Koch, Jan Christoph ^a   Bähr, Mathias ^a,c   Maina, Flavio ^b   Lingor, Paul ^a,c  

^a UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^b AIX MARSEILLE UNIVERSITÉ   (France)

^c Deutsche Forschungsgemeinschaft   (Germany)

Author keywords

axotomy; crush; HGF; optic nerve; regeneration; retinal ganglion cells

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; RECOMBINANT SCATTER FACTOR; SCATTER FACTOR; SCATTER FACTOR RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DEATH; CELL PROTECTION; CELL REGENERATION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NEUROPROTECTION; NONHUMAN; OPTIC NERVE INJURY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RAT; RETINA GANGLION CELL; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; AXONS; AXOTOMY; BLOTTING, WESTERN; CELL SURVIVAL; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; HEPATOCYTE GROWTH FACTOR; IN SITU HYBRIDIZATION; MICE; NERVE CRUSH; NERVE REGENERATION; NEURONS; NEUROPROTECTIVE AGENTS; OPTIC NERVE; OPTIC NERVE INJURIES; PROTO-ONCOGENE PROTEINS C-MET; RATS; RECOMBINANT PROTEINS; RETINAL GANGLION CELLS; SIGNAL TRANSDUCTION;

MURINAE; RATTUS;

EID: 79955668006     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2011.07257.x     Document Type: Article

References (41)

1. Bahr M., (2000) Live or let die-retinal ganglion cell death and survival during development and in the lesioned adult CNS. Trends Neurosci. 23, 483-490.
2. Barres B. A., Silverstein B. E., Corey D. P., and, Chun L. L., (1988) Immunological, morphological, and electrophysiological variation among retinal ganglion cells purified by panning. Neuron 1, 791-803.
3. Birchmeier C., and, Gherardi E., (1998) Developmental roles of HGF/SF and its receptor, the c-Met tyrosine kinase. Trends Cell Biol. 8, 404-410. (Pubitemid 28458706)
4. Borowiak M., Garratt A. N., Wustefeld T., Strehle M., Trautwein C., and, Birchmeier C., (2004) Met provides essential signals for liver regeneration. Proc. Natl Acad. Sci. USA 101, 10608-10613. (Pubitemid 38955789)
5. Bottaro D. P., Rubin J. S., Faletto D. L., Chan A. M., Kmiecik T. E., Vande Woude G. F., and, Aaronson S. A., (1991) Identification of the hepatocyte growth factor receptor as the c-met proto-oncogene product. Science 251, 802-804. (Pubitemid 21926175)
6. Coleman M. P., and, Perry V. H., (2002) Axon pathology in neurological disease: a neglected therapeutic target. Trends Neurosci. 25, 532-537. (Pubitemid 35246324)
7. Ebens A., Brose K., Leonardo E. D., Hanson M. G. Jr, Bladt F., Birchmeier C., Barres B. A., and, Tessier-Lavigne M., (1996) Hepatocyte growth factor/scatter factor is an axonal chemoattractant and a neurotrophic factor for spinal motor neurons. Neuron 17, 1157-1172. (Pubitemid 27021101)
8. Filbin M. T., (2003) Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat. Rev. Neurosci. 4, 703-713. (Pubitemid 37280150)
9. Fischer D., Petkova V., Thanos S., and, Benowitz L. I., (2004) Switching mature retinal ganglion cells to a robust growth state in vivo: gene expression and synergy with RhoA inactivation. J. Neurosci. 24, 8726-8740. (Pubitemid 39362968)
10. Giacobini P., Messina A., Wray S., Giampietro C., Crepaldi T., Carmeliet P., and, Fasolo A., (2007) Hepatocyte growth factor acts as a motogen and guidance signal for gonadotropin hormone-releasing hormone-1 neuronal migration. J. Neurosci. 27, 431-445. (Pubitemid 46106017)
11. Hamanoue M., Takemoto N., Matsumoto K., Nakamura T., Nakajima K., and, Kohsaka S., (1996) Neurotrophic effect of hepatocyte growth factor on central nervous system neurons in vitro. J. Neurosci. Res. 43, 554-564. (Pubitemid 26087390)
12. Helmbacher F., Dessaud E., Arber S., deLapeyriere O., Henderson C. E., Klein R., and, Maina F., (2003) Met signaling is required for recruitment of motor neurons to PEA3-positive motor pools. Neuron 39, 767-777. (Pubitemid 37088089)
13. Hossain M. A., Russell J. C., Gomez R., and, Laterra J., (2002) Neuroprotection by scatter factor/hepatocyte growth factor and FGF-1 in cerebellar granule neurons is phosphatidylinositol 3-kinase/akt-dependent and MAPK/CREB-independent. J. Neurochem. 81, 365-378. (Pubitemid 34809362)
14. Huh C. G., Factor V. M., Sanchez A., Uchida K., Conner E. A., and, Thorgeirsson S. S., (2004) Hepatocyte growth factor/c-met signaling pathway is required for efficient liver regeneration and repair. Proc. Natl Acad. Sci. USA 101, 4477-4482. (Pubitemid 38437436)
15. Kadoyama K., Funakoshi H., Ohya W., and, Nakamura T., (2007) Hepatocyte growth factor (HGF) attenuates gliosis and motoneuronal degeneration in the brainstem motor nuclei of a transgenic mouse model of ALS. Neurosci. Res. 59, 446-456. (Pubitemid 350007815)
16. Kadoyama K., Funakoshi H., Ohya-Shimada W., Nakamura T., Matsumoto K., and, Matsuyama S., (2009) Disease-dependent reciprocal phosphorylation of serine and tyrosine residues of c-Met/HGF receptor contributes disease retardation of a transgenic mouse model of ALS. Neurosci. Res. 65, 194-200.
17. Kato N., Nemoto K., Nakanishi K., Morishita R., Kaneda Y., Uenoyama M., Ikeda T., and, Fujikawa K., (2005) Nonviral HVJ (hemagglutinating virus of Japan) liposome-mediated retrograde gene transfer of human hepatocyte growth factor into rat nervous system promotes functional and histological recovery of the crushed nerve. Neurosci. Res. 52, 299-310. (Pubitemid 40917208)
18. Kitamura K., Iwanami A., Nakamura M., et al. (2007) Hepatocyte growth factor promotes endogenous repair and functional recovery after spinal cord injury. J. Neurosci. Res. 85, 2332-2342. (Pubitemid 47204748)
19. Knöferle J., Koch J. C., Ostendorf T., et al. (2010) Mechanisms of acute axonal degeneration in the optic nerve in vivo. Proc. Natl Acad. Sci. USA 107, 6064-6069.
20. Krishnamoorthy R. R., Agarwal P., Prasanna G., et al. (2001) Characterization of a transformed rat retinal ganglion cell line. Brain Res. Mol. Brain Res. 86, 1-12. (Pubitemid 32124753)
21. Lim C. S., and, Walikonis R. S., (2008) Hepatocyte growth factor and c-Met promote dendritic maturation during hippocampal neuron differentiation via the Akt pathway. Cell. Signal. 20, 825-835.
22. Lingor P., Tonges L., Pieper N., Bermel C., Barski E., Planchamp V., and, Bahr M., (2008) ROCK inhibition and CNTF interact on intrinsic signalling pathways and differentially regulate survival and regeneration in retinal ganglion cells. Brain 131, 250-263.
23. Machida S., Tanaka M., Ishii T., Ohtaka K., Takahashi T., and, Tazawa Y., (2004) Neuroprotective effect of hepatocyte growth factor against photoreceptor degeneration in rats. Invest. Ophthalmol. Vis. Sci. 45, 4174-4182. (Pubitemid 39411177)
24. Maina F., and, Klein R., (1999) Hepatocyte growth factor, a versatile signal for developing neurons. Nat. Neurosci. 2, 213-217. (Pubitemid 30491290)
25. Maina F., Casagranda F., Audero E., Simeone A., Comoglio P. M., Klein R., and, Ponzetto C., (1996) Uncoupling of Grb2 from the Met receptor in vivo reveals complex roles in muscle development. Cell 87, 531-542. (Pubitemid 26374326)
26. Maina F., Hilton M. C., Ponzetto C., Davies A. M., and, Klein R., (1997) Met receptor signaling is required for sensory nerve development and HGF promotes axonal growth and survival of sensory neurons. Genes Dev. 11, 3341-3350. (Pubitemid 28023958)
27. Maina F., Hilton M. C., Andres R., Wyatt S., Klein R., and, Davies A. M., (1998) Multiple roles for hepatocyte growth factor in sympathetic neuron development. Neuron 20, 835-846. (Pubitemid 28247390)
28. Maina F., Pante G., Helmbacher F., Andres R., Porthin A., Davies A. M., Ponzetto C., and, Klein R., (2001) Coupling Met to specific pathways results in distinct developmental outcomes. Mol. Cell 7, 1293-1306. (Pubitemid 32607362)
29. Miura Y., Yanagihara N., Imamura H., Kaida M., Moriwaki M., Shiraki K., and, Miki T., (2003) Hepatocyte growth factor stimulates proliferation and migration during wound healing of retinal pigment epithelial cells in vitro. Jpn. J. Ophthalmol. 47, 268-275. (Pubitemid 36627457)
30. Planchamp V., Bermel C., Tonges L., Ostendorf T., Kugler S., Reed J. C., Kermer P., Bahr M., and, Lingor P., (2008) BAG1 promotes axonal outgrowth and regeneration in vivo via Raf-1 and reduction of ROCK activity. Brain 131, 2606-2619.
31. Seigel G. M., and, Notter M. F., (1992) Lectin-induced differentiation of transformed neuroretinal cells in vitro. Exp. Cell Res. 199, 240-247.
32. Shi E., Jiang X., Kazui T., Washiyama N., Yamashita K., Terada H., and, Bashar A. H., (2006) Nonviral gene transfer of hepatocyte growth factor attenuates neurologic injury after spinal cord ischemia in rabbits. J. Thorac. Cardiovasc. Surg. 132, 941-947. (Pubitemid 44415892)
33. Shibuki H., Katai N., Kuroiwa S., Kurokawa T., Arai J., Matsumoto K., Nakamura T., and, Yoshimura N., (2002) Expression and neuroprotective effect of hepatocyte growth factor in retinal ischemia-reperfusion injury. Invest. Ophthalmol. Vis. Sci. 43, 528-536. (Pubitemid 34113239)
34. Sun W., Funakoshi H., and, Nakamura T., (1999) Differential expression of hepatocyte growth factor and its receptor, c-Met in the rat retina during development. Brain Res. 851, 46-53. (Pubitemid 30038128)
35. Sun W., Funakoshi H., and, Nakamura T., (2002) Overexpression of HGF retards disease progression and prolongs life span in a transgenic mouse model of ALS. J. Neurosci. 22, 6537-6548. (Pubitemid 35386410)
36. Thuret S., Alavian K. N., Gassmann M., Lloyd C. K., Smits S. M., Smidt M. P., Klein R., Dyck R. H., and, Simon H. H., (2004) The neuregulin receptor, ErbB4, is not required for normal development and adult maintenance of the substantia nigra pars compacta. J. Neurochem. 91, 1302-1311. (Pubitemid 39658557)
37. Van Bergen N. J., Wood J. P., Chidlow G., Trounce I. A., Casson R. J., Ju W. K., Weinreb R. N., and, Crowston J. G., (2009) Recharacterization of the RGC-5 retinal ganglion cell line. Invest. Ophthalmol. Vis. Sci. 50, 4267-4272.
38. Wong V., Glass D. J., Arriaga R., Yancopoulos G. D., Lindsay R. M., and, Conn G., (1997) Hepatocyte growth factor promotes motor neuron survival and synergizes with ciliary neurotrophic factor. J. Biol. Chem. 272, 5187-5191. (Pubitemid 27090077)
39. Xiao G. H., Jeffers M., Bellacosa A., Mitsuuchi Y., Vande Woude G. F., and, Testa J. R., (2001) Anti-apoptotic signaling by hepatocyte growth factor/Met via the phosphatidylinositol 3-kinase/Akt and mitogen-activated protein kinase pathways. Proc. Natl Acad. Sci. USA 98, 247-252. (Pubitemid 32095895)
40. Yamamoto Y., Livet J., Pollock R. A., Garces A., Arce V., deLapeyriere O., and, Henderson C. E., (1997) Hepatocyte growth factor (HGF/SF) is a muscle-derived survival factor for a subpopulation of embryonic motoneurons. Development 124, 2903-2913. (Pubitemid 27370906)
41. Zhang Y. W., Denham J., and, Thies R. S., (2006) Oligodendrocyte progenitor cells derived from human embryonic stem cells express neurotrophic factors. Stem Cells Dev. 15, 943-952. (Pubitemid 46147864)