DOI: 10.1242/dev.01209. HGF regulates the development of cortical pyramidal dendrites

HGF regulates the development of cortical pyramidal dendrites

10.1242/dev.01209

Crossref journal-article

The Company of Biologists

Development (237)

Abstract

Although hepatocyte growth factor (HGF) and its receptor tyrosine kinase MET are widely expressed in the developing and mature central nervous system,little is known about the role of MET signaling in the brain. We have used particle-mediated gene transfer in cortical organotypic slice cultures established from early postnatal mice to study the effects of HGF on the development of dendritic arbors of pyramidal neurons. Compared with untreated control cultures, exogenous HGF promoted a highly significant increase in dendritic growth and branching of layer 2 pyramidal neurons, whereas inactivation of endogenous HGF with function-blocking, anti-HGF antibody caused a marked reduction in size and complexity of the dendritic arbors of these neurons. Furthermore, pyramidal neurons transfected with an MET dominant-negative mutant receptor likewise had much smaller and less complex dendritic arbors than did control transfected neurons. Our results indicate that HGF plays a role in regulating dendritic morphology in the developing cerebral cortex.

Bibliography

Gutierrez, H., Dolcet, X., Tolcos, M., & Davies, A. (2004). HGF regulates the development of cortical pyramidal dendrites. Development, 131(15), 3717â3726.

Authors 4

Humberto Gutierrez (first)
Xavier Dolcet (additional)
Mary Tolcos (additional)
Alun Davies (additional)

References 42 Referenced 76

Dates

Type	When
Created	21 years, 1 month ago (June 30, 2004, 9:47 p.m.)
Deposited	4 years, 4 months ago (April 26, 2021, 2:10 a.m.)
Indexed	4 months, 2 weeks ago (April 8, 2025, 2:23 a.m.)
Issued	21 years ago (Aug. 1, 2004)
Published	21 years ago (Aug. 1, 2004)
Published Print	21 years ago (Aug. 1, 2004)

Funders 0

None

BibTeX

@article{Gutierrez_2004, title={HGF regulates the development of cortical pyramidal dendrites}, volume={131}, ISSN={0950-1991}, url={http://dx.doi.org/10.1242/dev.01209}, DOI={10.1242/dev.01209}, number={15}, journal={Development}, publisher={The Company of Biologists}, author={Gutierrez, Humberto and Dolcet, Xavier and Tolcos, Mary and Davies, Alun}, year={2004}, month=aug, pages={3717–3726} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        4,
        8
      ]
    ],
    "date-time": "2025-04-08T06:23:06Z",
    "timestamp": 1744093386124
  },
  "reference-count": 42,
  "publisher": "The Company of Biologists",
  "issue": "15",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2004,
        8,
        1
      ]
    ]
  },
  "abstract": "<jats:p>Although hepatocyte growth factor (HGF) and its receptor tyrosine kinase MET are widely expressed in the developing and mature central nervous system,little is known about the role of MET signaling in the brain. We have used particle-mediated gene transfer in cortical organotypic slice cultures established from early postnatal mice to study the effects of HGF on the development of dendritic arbors of pyramidal neurons. Compared with untreated control cultures, exogenous HGF promoted a highly significant increase in dendritic growth and branching of layer 2 pyramidal neurons, whereas inactivation of endogenous HGF with function-blocking, anti-HGF antibody caused a marked reduction in size and complexity of the dendritic arbors of these neurons. Furthermore, pyramidal neurons transfected with an MET dominant-negative mutant receptor likewise had much smaller and less complex dendritic arbors than did control transfected neurons. Our results indicate that HGF plays a role in regulating dendritic morphology in the developing cerebral cortex.</jats:p>",
  "DOI": "10.1242/dev.01209",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2004,
        7,
        1
      ]
    ],
    "date-time": "2004-07-01T01:47:15Z",
    "timestamp": 1088646435000
  },
  "page": "3717-3726",
  "source": "Crossref",
  "is-referenced-by-count": 76,
  "title": "HGF regulates the development of cortical pyramidal dendrites",
  "prefix": "10.1242",
  "volume": "131",
  "author": [
    {
      "given": "Humberto",
      "family": "Gutierrez",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Department Preclinical Veterinary Sciences, Royal (Dick) School of Veterinary Studies, University of Edinburgh, Summerhall Square, Edinburgh EH9 1QH,UK"
        }
      ]
    },
    {
      "given": "Xavier",
      "family": "Dolcet",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department Preclinical Veterinary Sciences, Royal (Dick) School of Veterinary Studies, University of Edinburgh, Summerhall Square, Edinburgh EH9 1QH,UK"
        }
      ]
    },
    {
      "given": "Mary",
      "family": "Tolcos",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department Preclinical Veterinary Sciences, Royal (Dick) School of Veterinary Studies, University of Edinburgh, Summerhall Square, Edinburgh EH9 1QH,UK"
        }
      ]
    },
    {
      "given": "Alun",
      "family": "Davies",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department Preclinical Veterinary Sciences, Royal (Dick) School of Veterinary Studies, University of Edinburgh, Summerhall Square, Edinburgh EH9 1QH,UK"
        }
      ]
    }
  ],
  "member": "237",
  "reference": [
    {
      "key": "2021042605072066100_REF1",
      "doi-asserted-by": "crossref",
      "unstructured": "Achim, C. L., Katyal, S., Wiley, C. A., Shiratori, M., Wang, G.,Oshika, E., Petersen, B. E., Li, J. M. and Michalopoulos, G. K.(1997). Expression of HGF and cMet in the developing and adult brain. Dev. Brain Res.102,299-303.",
      "DOI": "10.1016/S0165-3806(97)00108-9"
    },
    {
      "key": "2021042605072066100_REF2",
      "doi-asserted-by": "crossref",
      "unstructured": "Andermarcher, E., Surani, M. A. and Gherardi, E.(1996). Co-expression of the HGF/SF and c-met genes during early mouse embryogenesis precedes reciprocal expression in adjacent tissues during organogenesis. Dev. Genet.18,254-266.",
      "DOI": "10.1002/(SICI)1520-6408(1996)18:3<254::AID-DVG6>3.0.CO;2-8"
    },
    {
      "key": "2021042605072066100_REF3",
      "doi-asserted-by": "crossref",
      "unstructured": "Birchmeier, C. and Gherardi, E. (1998). Developmental role of HGF/SF and its receptor, the c-Met tyrosine kinase. Trends Cell Biol.8,404-410.",
      "DOI": "10.1016/S0962-8924(98)01359-2"
    },
    {
      "key": "2021042605072066100_REF4",
      "doi-asserted-by": "crossref",
      "unstructured": "Bladt, F., Riethmacher, D., Isenmann, S., Aguzzi, A. and Birchmeier, C. (1995). Essential role for the met receptor and the migration of myogenic precursor cells into the limb bud. Nature376,768-771.",
      "DOI": "10.1038/376768a0"
    },
    {
      "key": "2021042605072066100_REF5",
      "doi-asserted-by": "crossref",
      "unstructured": "Bonner-Fraser, M. (1995). Hepatocyte growth factor/scatter factor (HGF/SF) in early development: evidence for a role in neuronal induction. Trends Genet.11,423-425.",
      "DOI": "10.1016/S0168-9525(00)89136-2"
    },
    {
      "key": "2021042605072066100_REF6",
      "doi-asserted-by": "crossref",
      "unstructured": "Davey, F., Hilton, M. and Davies, A. M. (2000). Cooperation between HGF and CNTF in promoting the survival and growth of sensory and parasympathetic neurons. Mol. Cell. Neurosci.15,79-87.",
      "DOI": "10.1006/mcne.1999.0803"
    },
    {
      "key": "2021042605072066100_REF7",
      "doi-asserted-by": "crossref",
      "unstructured": "Davies, A. M. (2003). Regulation of neuronal survival and death by extracellular signals during development. EMBO J.22,2537-2545.",
      "DOI": "10.1093/emboj/cdg254"
    },
    {
      "key": "2021042605072066100_REF8",
      "unstructured": "Di Renzo, M. F., Bertolotto, A., Olivero, M., Putzolu, P.,Crepaldi, T., Schiffer, D., Pagni, C. A. and Comoglio, P. M.(1993). Selective expression of the Met/HGF receptor in human central nervous system microglia. Oncogene8, 219-222."
    },
    {
      "key": "2021042605072066100_REF9",
      "doi-asserted-by": "crossref",
      "unstructured": "Ebens, A., Brose, K., Leonardo, E. D., Hanson, M. G., 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. Neuron17,1157-1172.",
      "DOI": "10.1016/S0896-6273(00)80247-0"
    },
    {
      "key": "2021042605072066100_REF10",
      "unstructured": "Gherardi, E. and Stoker, M. (1991). Hepatocyte growth factor-scatter factor: mitogen, motogen and met. Cancer Cells3,227-232."
    },
    {
      "key": "2021042605072066100_REF11",
      "doi-asserted-by": "crossref",
      "unstructured": "Hamanoue, M., Tekemoto, N., Matsumoto, J., Nakamura, T.,Nakajima, K. and Kohsaka, S. (1996). Neurotrophic effect of hepatocyte growth factor on central nervous system in vitro. J. Neurosci. Res.43,554-564.",
      "DOI": "10.1002/(SICI)1097-4547(19960301)43:5<554::AID-JNR5>3.0.CO;2-H"
    },
    {
      "key": "2021042605072066100_REF12",
      "unstructured": "Hayar, T. F., Bambrick, L. L., Krueger, B. K. and Rakic, P.(1999). Organotypic slice cultures for analysis of proliferation,dell death, and migration in the embryonic neocortex. Brain Res. Brain Res. Protoc.4,425-437."
    },
    {
      "key": "2021042605072066100_REF13",
      "doi-asserted-by": "crossref",
      "unstructured": "Honda, S., Kagoshima, M., Wanaka, A., Tohoyama, M., Matsumoto,K. and Nakamura, T. (1995). Localization and functional coupling of HGF and c-met/HGF receptor in rat brain: implication as neurotrophic factor. Mol. Brain Res.32,197-210.",
      "DOI": "10.1016/0169-328X(95)00075-4"
    },
    {
      "key": "2021042605072066100_REF14",
      "doi-asserted-by": "crossref",
      "unstructured": "Horch, H. W., Kruttgen, A., Portbury, S. D. and Katz, L. C.(1999). Destabilization of cortical dendrites and spines by BDNF. Neuron23,353-364.",
      "DOI": "10.1016/S0896-6273(00)80785-0"
    },
    {
      "key": "2021042605072066100_REF15",
      "doi-asserted-by": "crossref",
      "unstructured": "Ieraci, A., Forni, P. E. and Ponzetto, C.(2002). Viable hypomorphic signaling mutant of the Met receptor reveals a role for hepatocyte growth factor in postnatal cerebellar development. Proc. Natl. Acad. Sci. USA99,15200-15205.",
      "DOI": "10.1073/pnas.222362099"
    },
    {
      "key": "2021042605072066100_REF16",
      "doi-asserted-by": "crossref",
      "unstructured": "Jung, W., Castren, E., Odenthal, M., VandeWoude, G. F., Ishii,T., Dienes, H. P. and Shirmacher, P. (1994). Expression and functional interaction of hepatocyte growth factor/scatter factor and its receptor c-met in mammalian brain. J. Cell Biol.126,485-494.",
      "DOI": "10.1083/jcb.126.2.485"
    },
    {
      "key": "2021042605072066100_REF17",
      "doi-asserted-by": "crossref",
      "unstructured": "Korhonen, L., Sjo\u0308holm, U., Takei, N., Kern, M. A.,Shirmacher, P., Castren, E. and Lindholm, D. (2000). Expression of c-Met in developing rat hippocampus: evidence for HGF as a neurotrophic factor for calbindin D-expressing neurons. Eur. J. Neurosci.12,3453-3461.",
      "DOI": "10.1046/j.1460-9568.2000.00260.x"
    },
    {
      "key": "2021042605072066100_REF18",
      "doi-asserted-by": "crossref",
      "unstructured": "Krasnoselsky, A., Massay, M. J., DeFrances, M. C.,Michalopoulos, G., Zarnegar, R. and Ratner, N. (1994). Hepatocyte growth factor is a mitogen for Schwann cells and is present in neurofibromas. J. Neurosci.14,7284-7290.",
      "DOI": "10.1523/JNEUROSCI.14-12-07284.1994"
    },
    {
      "key": "2021042605072066100_REF19",
      "doi-asserted-by": "crossref",
      "unstructured": "Maina, F. and Klein, R. (1999). Hepatocyte growth factor, a versatile signal for developing neurons. Nat. Neurosci.2,213-217.",
      "DOI": "10.1038/6310"
    },
    {
      "key": "2021042605072066100_REF20",
      "doi-asserted-by": "crossref",
      "unstructured": "Maina, F., Casagranda, F., Audero, E., Simeone, A., Comologlio,P. M., Klein, R. and Ponzetto, C. (1996). Ucoupling of Grb2 from the met receptor in vivo reveals complex roles in muscle development. Cell87,531-542.",
      "DOI": "10.1016/S0092-8674(00)81372-0"
    },
    {
      "key": "2021042605072066100_REF21",
      "doi-asserted-by": "crossref",
      "unstructured": "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. Neuron20,835-846.",
      "DOI": "10.1016/S0896-6273(00)80466-3"
    },
    {
      "key": "2021042605072066100_REF22",
      "doi-asserted-by": "crossref",
      "unstructured": "Maina, F., Hilton, M. C., Ponzetto, C., Davies, A. M. and Klein,R. (1997). Met receptor signalling is required for sensory nerve development. Genes Dev.11,3341-3350.",
      "DOI": "10.1101/gad.11.24.3341"
    },
    {
      "key": "2021042605072066100_REF23",
      "doi-asserted-by": "crossref",
      "unstructured": "Maina, F., Pante, G., Helmbacher, F., Andres, R., Porthin, A.,Davies, A. M., Ponzetto, C. and Klein, R. (2001). Coupling Met to specific pathways result in distinct developmental outcomes. Mol. Cell7,1293-1306.",
      "DOI": "10.1016/S1097-2765(01)00261-1"
    },
    {
      "key": "2021042605072066100_REF24",
      "doi-asserted-by": "crossref",
      "unstructured": "McAllister, A. K., Katz, L. C. and Lo, D. C.(1996). Neurotrophin regulation of cortical dendritic growth requires activity. Neuron17,1057-1064.",
      "DOI": "10.1016/S0896-6273(00)80239-1"
    },
    {
      "key": "2021042605072066100_REF25",
      "doi-asserted-by": "crossref",
      "unstructured": "McAllister, A. K., Katz, L. C. and Lo, D. C.(1997). Opposing role for endogenous BDNF and NT-3 in regulating cortical dendritic growth. Neuron18,767-778.",
      "DOI": "10.1016/S0896-6273(00)80316-5"
    },
    {
      "key": "2021042605072066100_REF26",
      "doi-asserted-by": "crossref",
      "unstructured": "McAllister, A. K., Lo, D. C. and Katz, L. W.(1995). Neurotrophins regulate dendritic grewth in developing visual cortex. Neuron15,791-803.",
      "DOI": "10.1016/0896-6273(95)90171-X"
    },
    {
      "key": "2021042605072066100_REF27",
      "doi-asserted-by": "crossref",
      "unstructured": "Miyazawa, T., Matsumoto, K., Ohmichi, H., Katoh, H., Yamashima,T. and Nakamura, T. (1998). Protection of hippocampal neurons from ischemia-induced delayed neuronal death by hepatocyte growth factor: a novel neurotrophic factor. J. Cereb. Blood Flow Metab.18,345-348.",
      "DOI": "10.1097/00004647-199804000-00001"
    },
    {
      "key": "2021042605072066100_REF28",
      "doi-asserted-by": "crossref",
      "unstructured": "Niblock, M. N., Brunso-Bechtold, J. K. and Riddle, D. R.(2000). Insuline-like growth factor I stimulates dendritic growth in primary somatosensory cortex. J. Neurosci.20,4165-4176.",
      "DOI": "10.1523/JNEUROSCI.20-11-04165.2000"
    },
    {
      "key": "2021042605072066100_REF29",
      "doi-asserted-by": "crossref",
      "unstructured": "Ponzzeto, C., Bardelli, A., Zhen, Z., Maina, F., dalla-Zonca,P., Giordano, S., Graziani, A., Panayotou, G. and Comoglio, P. M.(1994). A multifunctional Docking site medites signaling and transformation by the Hepatocyte Growth Factor/Scatter Factor receptor family. Cell77,261-271.",
      "DOI": "10.1016/0092-8674(94)90318-2"
    },
    {
      "key": "2021042605072066100_REF30",
      "doi-asserted-by": "crossref",
      "unstructured": "Powell, E. M., Mars, W. M. and Levitt, P.(2001). Hepatocyte growth factor/scatter factor is a motogen for interneurons migrating from the ventral to dorsal telencephalon. Neuron30,79-89.",
      "DOI": "10.1016/S0896-6273(01)00264-1"
    },
    {
      "key": "2021042605072066100_REF31",
      "doi-asserted-by": "crossref",
      "unstructured": "Schmidt, C., Bladt, F., Goedecke, S., Brinkmann, V., Zschiesche,W., Sharpe, M., Gherardi, E. and Birchmeier, C. (1995). Scatter factor/Hepatociyte growth factor is essential for liver development. Nature373,699-702.",
      "DOI": "10.1038/373699a0"
    },
    {
      "key": "2021042605072066100_REF32",
      "unstructured": "Sholl, D. A. (1953). Dendritic organization in the neurons of the visual and motor cortices of the cat. J. Anat.87,387-406."
    },
    {
      "key": "2021042605072066100_REF33",
      "doi-asserted-by": "crossref",
      "unstructured": "Sonnenberg, E., Meyer, D., Weidner, K. M. and Birchmeier, C.(1993). Scatter factor/hepatoycte growth factor and its receptor,the met tyrosine kinase, can mediate a signal exchange between mesenchyme and epithelia during mouse development. J. Cell Biol.123,223-235.",
      "DOI": "10.1083/jcb.123.1.223"
    },
    {
      "key": "2021042605072066100_REF34",
      "doi-asserted-by": "crossref",
      "unstructured": "Tan, J. C., Nocka, K., Ray, P., Traktman, P. and Besmer, P.(1990). The dominant W42 spotting phenotype results from a missense mutation in the c-kit receptor kinase. Science247,209-212.",
      "DOI": "10.1126/science.1688471"
    },
    {
      "key": "2021042605072066100_REF35",
      "doi-asserted-by": "crossref",
      "unstructured": "Thewke, D. P. and Seeds, N. W. (1999). The expression of mRNA for hepatocyte grewth factor/scatter factor, its receptor c-met, and one of its activators tissue-type plasminogen activator show a systematic relationship in the developing and adult cerebral cortex and hippocampus. Brain Res.821,356-367.",
      "DOI": "10.1016/S0006-8993(99)01115-4"
    },
    {
      "key": "2021042605072066100_REF36",
      "doi-asserted-by": "crossref",
      "unstructured": "Tsarfaty, I., Resau, J. H., Rulong, S., Keydar, U., Faletto, D. L. and VandeWoude, G. F. (1992). The met proto-oncogene receptor and lumen formation. Science257,1258-1261.",
      "DOI": "10.1126/science.1387731"
    },
    {
      "key": "2021042605072066100_REF37",
      "doi-asserted-by": "crossref",
      "unstructured": "Uehara, Y., Minowa, O., Mori, C., Shiota, K., Kuno, J., Noda, T. and Kitamura, N. (1995). Placental defect and embrionic lethality in mice lacking hepatocyte growth factor/Scatter factor. Nature373,702-705.",
      "DOI": "10.1038/373702a0"
    },
    {
      "key": "2021042605072066100_REF38",
      "doi-asserted-by": "crossref",
      "unstructured": "Whitford, K. L., Marillat, V., Stein, E., Goodman, C. S.,Tessier-Lavigne, M., Chedotail, A. and Ghosh, A. (2002). Regulation of cortical dendrite development by Slit-Robo interactions. Neuron22,47-61.",
      "DOI": "10.1016/S0896-6273(01)00566-9"
    },
    {
      "key": "2021042605072066100_REF39",
      "doi-asserted-by": "crossref",
      "unstructured": "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 synergises with ciliary neurotrophic factor. J. Biol. Chem.272,5187-5191.",
      "DOI": "10.1074/jbc.272.8.5187"
    },
    {
      "key": "2021042605072066100_REF40",
      "unstructured": "Yamamoto, Y., Livet, J., Vesjsada, R., Pollock, R. A., Arce, V.,delaPeyere, O., A. C. Kato and Henderson, C. E. (1997). Hepatocyte growth factor (HGF/SF) is an essential muscle derived survival factor for a subpopulation of embryonic motoneurons. Development124,2903-2913."
    },
    {
      "key": "2021042605072066100_REF41",
      "doi-asserted-by": "crossref",
      "unstructured": "Yang, X. M., Toma, J. G., Bamji, S. X., Velliveau, D. J., Khon,J., Park, M. and Miller, F. D. (1998). Autocrine hepatocyte greowth factor provides a local mechanism for promoting axonal growth. J. Neurosci.18,8369-8381.",
      "DOI": "10.1523/JNEUROSCI.18-20-08369.1998"
    },
    {
      "key": "2021042605072066100_REF42",
      "doi-asserted-by": "crossref",
      "unstructured": "Zhang, L., Himi, T., Morita, I. and Murota, S.(2000). Hepatocyte growth factor protects cultured rat cerebellar granule neurons via the phosphatidylinositol-3 kinase pathway/Akt pathway. J. Neurosci.59,489-496.",
      "DOI": "10.1002/(SICI)1097-4547(20000215)59:4<489::AID-JNR3>3.0.CO;2-9"
    }
  ],
  "container-title": "Development",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "http://journals.biologists.com/dev/article-pdf/131/15/3717/1147142/3717.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "http://journals.biologists.com/dev/article-pdf/131/15/3717/1147142/3717.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2021,
        4,
        26
      ]
    ],
    "date-time": "2021-04-26T06:10:27Z",
    "timestamp": 1619417427000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://journals.biologists.com/dev/article/131/15/3717/42524/HGF-regulates-the-development-of-cortical"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2004,
        8,
        1
      ]
    ]
  },
  "references-count": 42,
  "journal-issue": {
    "issue": "15",
    "published-print": {
      "date-parts": [
        [
          2004,
          8,
          1
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1242/dev.01209",
  "relation": {},
  "ISSN": [
    "1477-9129",
    "0950-1991"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        2004,
        8,
        1
      ]
    ]
  }
}