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Article ; Online: Use of Trowell-Type Organ Culture to Study Regulation of Dental Stem Cells.

Juuri, Emma / Balic, Anamaria

Journal of visualized experiments : JoVE

2021 , Issue 173

Abstract: Organ development, function, and regeneration depend on stem cells, which reside within discrete anatomical spaces called stem cell niches. The continuously growing mouse incisor provides an excellent model to study tissue-specific stem cells. The ... ...

Abstract	Organ development, function, and regeneration depend on stem cells, which reside within discrete anatomical spaces called stem cell niches. The continuously growing mouse incisor provides an excellent model to study tissue-specific stem cells. The epithelial tissue-specific stem cells of the incisor are located at the proximal end of the tooth in a niche called the cervical loop. They provide a continuous influx of cells to counterbalance the constant abrasion of the self-sharpening tip of the tooth. Presented here is a detailed protocol for the isolation and culture of the proximal end of the mouse incisor that houses stem cells and their niche. This is a modified Trowell-type organ culture protocol that enables in vitro culture of tissue pieces (explants), as well as the thick tissue slices at the liquid/air interface on a filter supported by a metal grid. The organ culture protocol described here enables tissue manipulations not feasible in vivo, and when combined with the use of a fluorescent reporter(s), it provides a platform for the identification and tracking of discrete cell populations in live tissues over time, including stem cells. Various regulatory molecules and pharmacological compounds can be tested in this system for their effect on stem cells and their niches. This ultimately provides a valuable tool to study stem cell regulation and maintenance.
MeSH term(s)	Animals ; Incisor ; Mice ; Organ Culture Techniques ; Stem Cell Niche ; Stem Cells
Language	English
Publishing date	2021-07-08
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Video-Audio Media
ZDB-ID	2259946-0
ISSN	1940-087X ; 1940-087X
ISSN (online)	1940-087X
ISSN	1940-087X
DOI	10.3791/62462
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Ptch2 is a Potential Regulator of Mesenchymal Stem Cells.

Juuri, Emma / Tikka, Pauli / Domanskyi, Andrii / Corfe, Ian / Morita, Wataru / Mckinnon, Peter J / Jandova, Nela / Balic, Anamaria

Frontiers in physiology

2022 Volume 13, Page(s) 877565

Abstract: Ptch receptors 1 and 2 mediate Hedgehog signaling pivotal for organ development and homeostasis. In contrast to embryonic ... ...

Abstract	Ptch receptors 1 and 2 mediate Hedgehog signaling pivotal for organ development and homeostasis. In contrast to embryonic lethal
Language	English
Publishing date	2022-04-28
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2564217-0
ISSN	1664-042X
ISSN	1664-042X
DOI	10.3389/fphys.2022.877565
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Article: Establishment of crown–root domain borders in mouse incisor

Juuri, Emma / Saito, Kan / Lefebvre, Sylvie / Michon, Frederic

Gene expression patterns. 2013 Oct., v. 13, no. 7

2013

Abstract: Teeth are composed of two domains, the enamel-covered crown and the enamel-free root. The understanding of the initiation and regulation of crown and root domain formation is important for the development of bioengineered teeth. In most teeth the crown ... ...

Abstract	Teeth are composed of two domains, the enamel-covered crown and the enamel-free root. The understanding of the initiation and regulation of crown and root domain formation is important for the development of bioengineered teeth. In most teeth the crown develops before the root, and erupts to the oral cavity whereas the root anchors the tooth to the jawbone. However, in the continuously growing mouse incisor the crown and root domains form simultaneously, the crown domain forming the labial and the root domain the lingual part of the tooth. While the crown–root border on the incisor distal side supports the distal enamel extent, reflecting an evolutionary diet adaptation, on the incisor mesial side the root-like surface is necessary for the attachment of the interdental ligament between the two incisors. Therefore, the mouse incisor exhibits a functional distal–mesial asymmetry. Here, we used the mouse incisor as a model to understand the mechanisms involved in the crown–root border formation. We analyzed the cellular origins and gene expression patterns leading to the development of the mesial and distal crown–root borders. We discovered that Barx2, En1, Wnt11, and Runx3 were exclusively expressed on the mesial crown–root border. In addition, the distal border of the crown–root domain might be established by cells from a different origin and by an early Follistatin expression, factor known to be involved in the root domain formation. The use of different mechanisms to establish domain borders gives indications of the incisor functional asymmetry.
Keywords	diet ; enamel ; follistatin ; gene expression regulation ; ligaments ; mice ; root crown ; teeth
Language	English
Dates of publication	2013-10
Size	p. 255-264.
Publishing place	Elsevier B.V.
Document type	Article
ZDB-ID	2058346-1
ISSN	1872-7298 ; 1567-133X
ISSN (online)	1872-7298
ISSN	1567-133X
DOI	10.1016/j.gep.2013.05.001
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Article ; Online: Mesenchymal Wnt/β-Catenin Signaling Controls Epithelial Stem Cell Homeostasis in Teeth by Inhibiting the Antiapoptotic Effect of Fgf10.

Yang, Zheqiong / Balic, Anamaria / Michon, Frederic / Juuri, Emma / Thesleff, Irma

Stem cells (Dayton, Ohio)

2015 Volume 33, Issue 5, Page(s) 1670–1681

Abstract: Continuous growth of rodent incisors relies on epithelial stem cells (SCs) located in the SC niche called labial cervical loop (LaCL). Here, we found a population of apoptotic cells residing in a specific location of the LaCL in mouse incisor. Activated ... ...

Abstract	Continuous growth of rodent incisors relies on epithelial stem cells (SCs) located in the SC niche called labial cervical loop (LaCL). Here, we found a population of apoptotic cells residing in a specific location of the LaCL in mouse incisor. Activated Caspase 3 and Caspase 9, expressed in this location colocalized in part with Lgr5 in putative SCs. The addition of Caspase inhibitors to incisors ex vivo resulted in concentration dependent thickening of LaCL. To examine the role of Wnt signaling in regulation of apoptosis, we exposed the LaCL of postnatal day 2 (P2) mouse incisor ex vivo to BIO, a known activator of Wnt/β-catenin signaling. This resulted in marked thinning of LaCL as well as enhanced apoptosis. We found that Wnt/β-catenin signaling was intensely induced by BIO in the mesenchyme surrounding the LaCL, but, unexpectedly, no β-catenin activity was detected in the LaCL epithelium either before or after BIO treatment. We discovered that the expression of Fgf10, an essential growth factor for incisor epithelial SCs, was dramatically downregulated in the mesenchyme around BIO-treated LaCL, and that exogenous Fgf10 could rescue the thinning of the LaCL caused by BIO. We conclude that the homeostasis of the epithelial SC population in the mouse incisor depends on a proper rate of apoptosis and that this apoptosis is controlled by signals from the mesenchyme surrounding the LaCL. Fgf10 is a key mesenchymal signal limiting apoptosis of incisor epithelial SCs and its expression is negatively regulated by Wnt/β-catenin. Stem Cells 2015;33:1670-1681.
MeSH term(s)	Animals ; Apoptosis/drug effects ; Cell Proliferation/drug effects ; Epithelial Cells/cytology ; Epithelial Cells/drug effects ; Fibroblast Growth Factor 10/pharmacology ; Homeostasis/drug effects ; Incisor/cytology ; Mesoderm/drug effects ; Mesoderm/metabolism ; Mice ; Models, Biological ; Receptors, G-Protein-Coupled/metabolism ; Stem Cell Niche/drug effects ; Stem Cells/cytology ; Stem Cells/drug effects ; Stem Cells/metabolism ; Tooth/cytology ; Wnt Signaling Pathway/drug effects
Chemical Substances	Fibroblast Growth Factor 10 ; Lgr5 protein, mouse ; Receptors, G-Protein-Coupled
Language	English
Publishing date	2015-05
Publishing country	United States
Document type	Journal Article
ZDB-ID	1143556-2
ISSN	1549-4918 ; 1066-5099
ISSN (online)	1549-4918
ISSN	1066-5099
DOI	10.1002/stem.1972
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Article ; Online: Establishment of crown-root domain borders in mouse incisor.

Juuri, Emma / Saito, Kan / Lefebvre, Sylvie / Michon, Frederic

Gene expression patterns : GEP

2013 Volume 13, Issue 7, Page(s) 255–264

Abstract	Teeth are composed of two domains, the enamel-covered crown and the enamel-free root. The understanding of the initiation and regulation of crown and root domain formation is important for the development of bioengineered teeth. In most teeth the crown develops before the root, and erupts to the oral cavity whereas the root anchors the tooth to the jawbone. However, in the continuously growing mouse incisor the crown and root domains form simultaneously, the crown domain forming the labial and the root domain the lingual part of the tooth. While the crown-root border on the incisor distal side supports the distal enamel extent, reflecting an evolutionary diet adaptation, on the incisor mesial side the root-like surface is necessary for the attachment of the interdental ligament between the two incisors. Therefore, the mouse incisor exhibits a functional distal-mesial asymmetry. Here, we used the mouse incisor as a model to understand the mechanisms involved in the crown-root border formation. We analyzed the cellular origins and gene expression patterns leading to the development of the mesial and distal crown-root borders. We discovered that Barx2, En1, Wnt11, and Runx3 were exclusively expressed on the mesial crown-root border. In addition, the distal border of the crown-root domain might be established by cells from a different origin and by an early Follistatin expression, factor known to be involved in the root domain formation. The use of different mechanisms to establish domain borders gives indications of the incisor functional asymmetry.
MeSH term(s)	Ameloblasts/metabolism ; Ameloblasts/physiology ; Animals ; Dental Enamel/growth & development ; Dental Enamel/metabolism ; Follistatin/genetics ; Follistatin/metabolism ; Gene Expression Profiling ; Gene Expression Regulation, Developmental ; Imaging, Three-Dimensional ; Incisor/growth & development ; Mice ; Mice, Knockout ; Morphogenesis ; Odontogenesis ; Tooth Crown/growth & development ; Tooth Crown/metabolism ; Tooth Root/growth & development ; Tooth Root/metabolism
Chemical Substances	Follistatin
Language	English
Publishing date	2013-10
Publishing country	Netherlands
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2058346-1
ISSN	1872-7298 ; 1567-133X
ISSN (online)	1872-7298
ISSN	1567-133X
DOI	10.1016/j.gep.2013.05.001
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Expression of the stem cell marker, SOX2, in ameloblastoma and dental epithelium.

Juuri, Emma / Isaksson, Sanna / Jussila, Maria / Heikinheimo, Kristiina / Thesleff, Irma

European journal of oral sciences

2013 Volume 121, Issue 6, Page(s) 509–516

Abstract: Ameloblastomas are locally invasive odontogenic tumors that exhibit a high rate of recurrence and often associate with the third molars. They are suggested to originate from dental epithelium because the tumor cells resemble epithelial cells of ... ...

Abstract	Ameloblastomas are locally invasive odontogenic tumors that exhibit a high rate of recurrence and often associate with the third molars. They are suggested to originate from dental epithelium because the tumor cells resemble epithelial cells of developing teeth. Expression of the transcription factor SOX2 has been previously localized in epithelial stem and progenitor cells in developing teeth as well as in various tumors. Here, we show that SOX2 is expressed in the epithelial cells of follicular and plexiform ameloblastomas. SOX2 was localized in the dental lamina of developing human primary molars. It was also expressed in the fragmented dental lamina associated with the third molars and in the epithelium budding from its posterior aspect in mice. However, no SOX2 expression was detected in either Hertwig's epithelial root sheath directing the formation of roots or in the epithelial cell rests of Malassez covering the completed roots. SOX2 was associated with supernumerary tooth formation in odontoma-like tumors induced by Wnt signal activation in mice. We propose that SOX2 functions in maintaining the progenitor state of epithelium in ameloblastomas and that ameloblastomas may originate from SOX2-expressing dental lamina epithelium.
MeSH term(s)	Adolescent ; Adult ; Aged ; Ameloblastoma/metabolism ; Ameloblastoma/pathology ; Animals ; Biomarkers/metabolism ; Epithelium/metabolism ; Epithelium/pathology ; Female ; Humans ; In Situ Hybridization ; Jaw Neoplasms/metabolism ; Jaw Neoplasms/pathology ; Male ; Mandible/pathology ; Mice ; Mice, Mutant Strains ; Middle Aged ; Molar, Third/growth & development ; Molar, Third/metabolism ; Odontogenesis/physiology ; Odontogenic Tumors/metabolism ; Odontogenic Tumors/pathology ; RNA, Messenger/metabolism ; SOXB1 Transcription Factors/metabolism ; Stem Cells/metabolism ; Tooth Root/growth & development ; Tooth Root/metabolism ; Tooth, Supernumerary/embryology ; Wnt Signaling Pathway/physiology
Chemical Substances	Biomarkers ; RNA, Messenger ; SOXB1 Transcription Factors
Language	English
Publishing date	2013-12
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1224820-4
ISSN	1600-0722 ; 0909-8836
ISSN (online)	1600-0722
ISSN	0909-8836
DOI	10.1111/eos.12095
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Article ; Online: Sox2+ stem cells contribute to all epithelial lineages of the tooth via Sfrp5+ progenitors.

Juuri, Emma / Saito, Kan / Ahtiainen, Laura / Seidel, Kerstin / Tummers, Mark / Hochedlinger, Konrad / Klein, Ophir D / Thesleff, Irma / Michon, Frederic

Developmental cell

2012 Volume 23, Issue 2, Page(s) 317–328

Abstract: The continuously growing mouse incisor serves as a valuable model to study stem cell regulation during organ renewal. Epithelial stem cells are localized in the proximal end of the incisor in the labial cervical loop. Here, we show that the transcription ...

Abstract	The continuously growing mouse incisor serves as a valuable model to study stem cell regulation during organ renewal. Epithelial stem cells are localized in the proximal end of the incisor in the labial cervical loop. Here, we show that the transcription factor Sox2 is a specific marker for these stem cells. Sox2+ cells became restricted to the labial cervical loop during tooth morphogenesis, and they contributed to the renewal of enamel-producing ameloblasts as well as all other epithelial cell lineages of the tooth. The early progeny of Sox2-positive stem cells transiently expressed the Wnt inhibitor Sfrp5. Sox2 expression was regulated by the tooth initiation marker FGF8 and specific miRNAs, suggesting a fine-tuning to maintain homeostasis of the dental epithelium. The identification of Sox2 as a marker for the dental epithelial stem cells will facilitate further studies on their lineage segregation and differentiation during tooth renewal.
MeSH term(s)	Adaptor Proteins, Signal Transducing ; Animals ; Biomarkers/analysis ; Biomarkers/metabolism ; Cell Differentiation ; Cell Lineage ; Cells, Cultured ; Epithelial Cells/chemistry ; Epithelial Cells/cytology ; Epithelial Cells/metabolism ; Fibroblast Growth Factor 8/genetics ; Gene Expression Regulation, Developmental ; Intercellular Signaling Peptides and Proteins/metabolism ; Mice ; MicroRNAs/genetics ; Organ Culture Techniques ; SOXB1 Transcription Factors/analysis ; SOXB1 Transcription Factors/biosynthesis ; Stem Cells/chemistry ; Stem Cells/cytology ; Stem Cells/metabolism ; Tooth/cytology ; Tooth/embryology ; Tooth/growth & development ; Tooth/metabolism
Chemical Substances	Adaptor Proteins, Signal Transducing ; Biomarkers ; Fgf8 protein, mouse ; Intercellular Signaling Peptides and Proteins ; MicroRNAs ; SOXB1 Transcription Factors ; Sfrp5 protein, mouse ; Sox2 protein, mouse ; Fibroblast Growth Factor 8 (148997-75-5)
Language	English
Publishing date	2012-07-19
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2054967-2
ISSN	1878-1551 ; 1534-5807
ISSN (online)	1878-1551
ISSN	1534-5807
DOI	10.1016/j.devcel.2012.05.012
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Article: Sox2+ Stem Cells Contribute to All Epithelial Lineages of the Tooth via Sfrp5+ Progenitors

Juuri, Emma / Saito, Kan / Ahtiainen, Laura / Seidel, Kerstin / Tummers, Mark / Hochedlinger, Konrad / Klein, Ophir D / Thesleff, Irma / Michon, Frederic

Developmental cell. 2012 Aug. 14, v. 23, no. 2

2012

Abstract	The continuously growing mouse incisor serves as a valuable model to study stem cell regulation during organ renewal. Epithelial stem cells are localized in the proximal end of the incisor in the labial cervical loop. Here, we show that the transcription factor Sox2 is a specific marker for these stem cells. Sox2+ cells became restricted to the labial cervical loop during tooth morphogenesis, and they contributed to the renewal of enamel-producing ameloblasts as well as all other epithelial cell lineages of the tooth. The early progeny of Sox2-positive stem cells transiently expressed the Wnt inhibitor Sfrp5. Sox2 expression was regulated by the tooth initiation marker FGF8 and specific miRNAs, suggesting a fine-tuning to maintain homeostasis of the dental epithelium. The identification of Sox2 as a marker for the dental epithelial stem cells will facilitate further studies on their lineage segregation and differentiation during tooth renewal.
Keywords	epithelial cells ; epithelium ; homeostasis ; mice ; microRNA ; models ; morphogenesis ; progeny ; stem cells ; transcription factors
Language	English
Dates of publication	2012-0814
Size	p. 317-328.
Publishing place	Elsevier Inc.
Document type	Article
ZDB-ID	2054967-2
ISSN	1878-1551 ; 1534-5807
ISSN (online)	1878-1551
ISSN	1534-5807
DOI	10.1016/j.devcel.2012.05.012
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Article ; Online: Sox2 marks epithelial competence to generate teeth in mammals and reptiles.

Juuri, Emma / Jussila, Maria / Seidel, Kerstin / Holmes, Scott / Wu, Ping / Richman, Joy / Heikinheimo, Kristiina / Chuong, Cheng-Ming / Arnold, Katrin / Hochedlinger, Konrad / Klein, Ophir / Michon, Frederic / Thesleff, Irma

Development (Cambridge, England)

2013 Volume 140, Issue 7, Page(s) 1424–1432

Abstract: Tooth renewal is initiated from epithelium associated with existing teeth. The development of new teeth requires dental epithelial cells that have competence for tooth formation, but specific marker genes for these cells have not been identified. Here, ... ...

Abstract	Tooth renewal is initiated from epithelium associated with existing teeth. The development of new teeth requires dental epithelial cells that have competence for tooth formation, but specific marker genes for these cells have not been identified. Here, we analyzed expression patterns of the transcription factor Sox2 in two different modes of successional tooth formation: tooth replacement and serial addition of primary teeth. We observed specific Sox2 expression in the dental lamina that gives rise to successional teeth in mammals with one round of tooth replacement as well as in reptiles with continuous tooth replacement. Sox2 was also expressed in the dental lamina during serial addition of mammalian molars, and genetic lineage tracing indicated that Sox2(+) cells of the first molar give rise to the epithelial cell lineages of the second and third molars. Moreover, conditional deletion of Sox2 resulted in hyperplastic epithelium in the forming posterior molars. Our results indicate that the Sox2(+) dental epithelium has competence for successional tooth formation and that Sox2 regulates the progenitor state of dental epithelial cells. The findings imply that the function of Sox2 has been conserved during evolution and that tooth replacement and serial addition of primary teeth represent variations of the same developmental process. The expression patterns of Sox2 support the hypothesis that dormant capacity for continuous tooth renewal exists in mammals.
MeSH term(s)	Animals ; Biomarkers/metabolism ; Cells, Cultured ; Embryo, Mammalian ; Epithelial Cells/metabolism ; Female ; Ferrets ; Humans ; Mammals/embryology ; Mammals/genetics ; Mammals/growth & development ; Mice ; Mice, Transgenic ; Models, Biological ; Pregnancy ; Regeneration/genetics ; Regeneration/physiology ; Reptiles/genetics ; Reptiles/growth & development ; SOXB1 Transcription Factors/genetics ; SOXB1 Transcription Factors/metabolism ; SOXB1 Transcription Factors/physiology ; Tooth/embryology ; Tooth/growth & development ; Tooth/metabolism ; Tooth/physiology
Chemical Substances	Biomarkers ; SOXB1 Transcription Factors
Language	English
Publishing date	2013-03-05
Publishing country	England
Document type	Comparative Study ; Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	90607-4
ISSN	1477-9129 ; 0950-1991
ISSN (online)	1477-9129
ISSN	0950-1991
DOI	10.1242/dev.089599
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Article: Establishment of crownâroot domain borders in mouse incisor

Juuri, Emma / Kan SaitoauthorInstitute of Biotechnology, Developmental Biology Program, University of Helsinki, 00014 Helsinki, Finland / Sylvie LefebvreauthorInstitute of Biotechnology, Developmental Biology Program, University of Helsinki, 00014 Helsinki, Finland / Frederic MichonauthorInstitute of Biotechnology, Developmental Biology Program, University of Helsinki, 00014 Helsinki, Finland. Electronic address: Frederic.Michon@helsinki.fi

Language	English
Document type	Article
Database	AGRIS - International Information System for the Agricultural Sciences and Technology

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