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Article ; Online: New developments in the biology of fibroblast growth factors.

Ornitz, David M / Itoh, Nobuyuki

WIREs mechanisms of disease

2022 Volume 14, Issue 4, Page(s) e1549

Abstract: The fibroblast growth factor (FGF) family is composed of 18 secreted signaling proteins consisting of canonical FGFs and endocrine FGFs that activate four receptor tyrosine kinases (FGFRs 1-4) and four intracellular proteins (intracellular FGFs or iFGFs) ...

Abstract	The fibroblast growth factor (FGF) family is composed of 18 secreted signaling proteins consisting of canonical FGFs and endocrine FGFs that activate four receptor tyrosine kinases (FGFRs 1-4) and four intracellular proteins (intracellular FGFs or iFGFs) that primarily function to regulate the activity of voltage-gated sodium channels and other molecules. The canonical FGFs, endocrine FGFs, and iFGFs have been reviewed extensively by us and others. In this review, we briefly summarize past reviews and then focus on new developments in the FGF field since our last review in 2015. Some of the highlights in the past 6 years include the use of optogenetic tools, viral vectors, and inducible transgenes to experimentally modulate FGF signaling, the clinical use of small molecule FGFR inhibitors, an expanded understanding of endocrine FGF signaling, functions for FGF signaling in stem cell pluripotency and differentiation, roles for FGF signaling in tissue homeostasis and regeneration, a continuing elaboration of mechanisms of FGF signaling in development, and an expanding appreciation of roles for FGF signaling in neuropsychiatric diseases. This article is categorized under: Cardiovascular Diseases > Molecular and Cellular Physiology Neurological Diseases > Molecular and Cellular Physiology Congenital Diseases > Stem Cells and Development Cancer > Stem Cells and Development.
MeSH term(s)	Biology ; Fibroblast Growth Factors/genetics ; Receptor Protein-Tyrosine Kinases/metabolism ; Receptors, Fibroblast Growth Factor/genetics ; Signal Transduction
Chemical Substances	Receptors, Fibroblast Growth Factor ; Fibroblast Growth Factors (62031-54-3) ; Receptor Protein-Tyrosine Kinases (EC 2.7.10.1)
Language	English
Publishing date	2022-02-09
Publishing country	United States
Document type	Journal Article ; Review ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ISSN	2692-9368
ISSN (online)	2692-9368
DOI	10.1002/wsbm.1549
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Article ; Online: FGF9 and FGF10 activate distinct signaling pathways to direct lung epithelial specification and branching.

Yin, Yongjun / Ornitz, David M

Science signaling

2020 Volume 13, Issue 621

Abstract: Fibroblast growth factors (FGFs) 9 and 10 are essential during the pseudoglandular stage of lung development. Mesothelium-produced FGF9 is principally responsible for mesenchymal growth, whereas epithelium-produced FGF9 and mesenchyme-produced FGF10 ... ...

Abstract	Fibroblast growth factors (FGFs) 9 and 10 are essential during the pseudoglandular stage of lung development. Mesothelium-produced FGF9 is principally responsible for mesenchymal growth, whereas epithelium-produced FGF9 and mesenchyme-produced FGF10 guide lung epithelial development, and loss of either of these ligands affects epithelial branching. Because FGF9 and FGF10 activate distinct FGF receptors (FGFRs), we hypothesized that they would control distinct developmental processes. Here, we found that FGF9 signaled through epithelial FGFR3 to directly promote distal epithelial fate specification and inhibit epithelial differentiation. By contrast, FGF10 signaled through epithelial FGFR2b to promote epithelial proliferation and differentiation. Furthermore, FGF9-FGFR3 signaling functionally opposed FGF10-FGFR2b signaling, and FGFR3 preferentially used downstream phosphoinositide 3-kinase (PI3K) pathways, whereas FGFR2b relied on downstream mitogen-activated protein kinase (MAPK) pathways. These data demonstrate that, within lung epithelial cells, different FGFRs function independently; they bind receptor-specific ligands and direct distinct developmental functions through the activation of distinct downstream signaling pathways.
MeSH term(s)	Animals ; Epithelial Cells/metabolism ; Fibroblast Growth Factor 10/genetics ; Fibroblast Growth Factor 10/metabolism ; Fibroblast Growth Factor 9/genetics ; Fibroblast Growth Factor 9/metabolism ; Lung/cytology ; Lung/embryology ; Mice ; Mice, Transgenic ; Signal Transduction
Chemical Substances	Fgf10 protein, mouse ; Fgf9 protein, mouse ; Fibroblast Growth Factor 10 ; Fibroblast Growth Factor 9
Language	English
Publishing date	2020-03-03
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2417226-1
ISSN	1937-9145 ; 1945-0877
ISSN (online)	1937-9145
ISSN	1945-0877
DOI	10.1126/scisignal.aay4353
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Article ; Online: Fibroblast growth factors in skeletal development.

Ornitz, David M / Marie, Pierre J

Current topics in developmental biology

2019 Volume 133, Page(s) 195–234

Abstract: Fibroblast growth factors (FGFs) and their receptors (FGFRs) are expressed throughout all stages of skeletal development. In the limb bud and in cranial mesenchyme, FGF signaling is important for formation of mesenchymal condensations that give rise to ... ...

Abstract	Fibroblast growth factors (FGFs) and their receptors (FGFRs) are expressed throughout all stages of skeletal development. In the limb bud and in cranial mesenchyme, FGF signaling is important for formation of mesenchymal condensations that give rise to bone. Once skeletal elements are initiated and patterned, FGFs regulate both endochondral and intramembranous ossification programs. In this chapter, we review functions of the FGF signaling pathway during these critical stages of skeletogenesis, and explore skeletal malformations in humans that are caused by mutations in FGF signaling molecules.
MeSH term(s)	Animals ; Bone Diseases/genetics ; Chondrocytes/metabolism ; Fibroblast Growth Factors/metabolism ; Humans ; Osteogenesis ; Receptors, Fibroblast Growth Factor/genetics ; Receptors, Fibroblast Growth Factor/metabolism ; Signal Transduction
Chemical Substances	Receptors, Fibroblast Growth Factor ; Fibroblast Growth Factors (62031-54-3)
Language	English
Publishing date	2019-01-03
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ISSN	1557-8933 ; 0070-2153
ISSN (online)	1557-8933
ISSN	0070-2153
DOI	10.1016/bs.ctdb.2018.11.020
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Article ; Online: Identification of a myofibroblast differentiation program during neonatal lung development.

Yin, Yongjun / Koenitzer, Jeffrey R / Patra, Debabrata / Dietmann, Sabine / Bayguinov, Peter / Hagan, Andrew S / Ornitz, David M

Development (Cambridge, England)

2024

Abstract: Alveologenesis is the final stage of lung development in which the internal surface area of the lung is increased to facilitate efficient gas exchange in the mature organism. The first phase of alveologenesis involves the formation of septal ridges ( ... ...

Abstract	Alveologenesis is the final stage of lung development in which the internal surface area of the lung is increased to facilitate efficient gas exchange in the mature organism. The first phase of alveologenesis involves the formation of septal ridges (secondary septae) and the second phase involves thinning of the alveolar septa. Within secondary septa, mesenchymal cells include a transient population of alveolar myofibroblasts (MyoFB) and a stable but poorly described population of lipid rich cells that have been referred to as lipofibroblasts or matrix fibroblasts (MatFB). Using a unique Fgf18CreER lineage trace mouse line, cell sorting, single cell RNA sequencing, and primary cell culture, we have identified multiple subtypes of mesenchymal cells in the neonatal lung, including an immature progenitor cell that gives rise to mature MyoFB. We also show that the endogenous and targeted ROSA26 locus serves as a sensitive reporter for MyoFB maturation. These studies identify a MyoFB differentiation program that is distinct from other mesenchymal cell types and increases the known repertoire of mesenchymal cell types in the neonatal lung.
Language	English
Publishing date	2024-04-11
Publishing country	England
Document type	Journal Article
ZDB-ID	90607-4
ISSN	1477-9129 ; 0950-1991
ISSN (online)	1477-9129
ISSN	0950-1991
DOI	10.1242/dev.202659
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Article ; Online: Targeted deletion of Fgf9 in tendon disrupts mineralization of the developing enthesis.

Ganji, Elahe / Leek, Connor / Duncan, William / Patra, Debabrata / Ornitz, David M / Killian, Megan L

FASEB journal : official publication of the Federation of American Societies for Experimental Biology

2023 Volume 37, Issue 3, Page(s) e22777

Abstract: The enthesis is a transitional tissue between tendon and bone that matures postnatally. The development and maturation of the enthesis involve cellular processes likened to an arrested growth plate. In this study, we explored the role of fibroblast ... ...

Abstract	The enthesis is a transitional tissue between tendon and bone that matures postnatally. The development and maturation of the enthesis involve cellular processes likened to an arrested growth plate. In this study, we explored the role of fibroblast growth factor 9 (Fgf9), a known regulator of chondrogenesis and vascularization during bone development, on the structure and function of the postnatal enthesis. First, we confirmed spatial expression of Fgf9 in the tendon and enthesis using in situ hybridization. We then used Cre-lox recombinase to conditionally knockout Fgf9 in mouse tendon and enthesis (Scx-Cre) and characterized enthesis morphology as well as mechanical properties in Fgf9
MeSH term(s)	Mice ; Animals ; Fibroblast Growth Factor 9/genetics ; Fibroblast Growth Factor 9/metabolism ; Tendons/metabolism ; Bone and Bones ; Bone Development/genetics ; Chondrogenesis
Chemical Substances	Fibroblast Growth Factor 9 ; Fgf9 protein, mouse
Language	English
Publishing date	2023-01-30
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	639186-2
ISSN	1530-6860 ; 0892-6638
ISSN (online)	1530-6860
ISSN	0892-6638
DOI	10.1096/fj.202201614R
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Article ; Online: Sculpting the skull through neurosensory epithelial-mesenchymal signaling.

Yang, Lu M / Ornitz, David M

Developmental dynamics : an official publication of the American Association of Anatomists

2018 Volume 248, Issue 1, Page(s) 88–97

Abstract: The vertebrate skull is a complex structure housing the brain and specialized sensory organs, including the eye, the inner ear, and the olfactory system. The close association between bones of the skull and the sensory organs they encase has posed ... ...

Abstract	The vertebrate skull is a complex structure housing the brain and specialized sensory organs, including the eye, the inner ear, and the olfactory system. The close association between bones of the skull and the sensory organs they encase has posed interesting developmental questions about how the tissues scale with one another. Mechanisms that regulate morphogenesis of the skull are hypothesized to originate in part from the encased neurosensory organs. Conversely, the developing skull is hypothesized to regulate the growth of neurosensory organs, through mechanical forces or molecular signaling. Here, we review studies of epithelial-mesenchymal interactions during inner ear and olfactory system development that may coordinate the growth of the two sensory organs with their surrounding bone. We highlight recent progress in the field and provide evidence that mechanical forces arising from bone growth may affect olfactory epithelium development. Developmental Dynamics 248:88-97, 2019. © 2018 Wiley Periodicals, Inc.
MeSH term(s)	Animals ; Ear, Inner/growth & development ; Epithelium/growth & development ; Epithelium/metabolism ; Humans ; Mechanical Phenomena ; Mesoderm/metabolism ; Olfactory Bulb/growth & development ; Signal Transduction ; Skull/anatomy & histology ; Vertebrates/anatomy & histology
Language	English
Publishing date	2018-09-24
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	1102541-4
ISSN	1097-0177 ; 1058-8388
ISSN (online)	1097-0177
ISSN	1058-8388
DOI	10.1002/dvdy.24664
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Article ; Online: Identification of a FGF18-expressing alveolar myofibroblast that is developmentally cleared during alveologenesis.

Hagan, Andrew S / Zhang, Bo / Ornitz, David M

Development (Cambridge, England)

2020 Volume 147, Issue 2

Abstract: Alveologenesis is an essential developmental process that increases the surface area of the lung through the formation of septal ridges. In the mouse, septation occurs postnatally and is thought to require the alveolar myofibroblast (AMF). Though ... ...

Abstract	Alveologenesis is an essential developmental process that increases the surface area of the lung through the formation of septal ridges. In the mouse, septation occurs postnatally and is thought to require the alveolar myofibroblast (AMF). Though abundant during alveologenesis, markers for AMFs are minimally detected in the adult. After septation, the alveolar walls thin to allow efficient gas exchange. Both loss of AMFs or retention and differentiation into another cell type during septal thinning have been proposed. Using a novel
MeSH term(s)	Animals ; Animals, Newborn ; Cell Lineage ; Fibroblast Growth Factors/genetics ; Fibroblast Growth Factors/metabolism ; Gene Expression Regulation, Developmental ; Mesoderm/cytology ; Mice, Inbred C57BL ; Models, Biological ; Myofibroblasts/cytology ; Myofibroblasts/metabolism ; Organogenesis ; Phagocytosis ; Pulmonary Alveoli/growth & development ; Time Factors
Chemical Substances	fibroblast growth factor 18 ; Fibroblast Growth Factors (62031-54-3)
Language	English
Publishing date	2020-01-17
Publishing country	England
Document type	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.181032
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Article ; Online: FGF20-FGFR1 signaling through MAPK and PI3K controls sensory progenitor differentiation in the organ of Corti.

Su, Yutao / Yang, Lu M / Ornitz, David M

Developmental dynamics : an official publication of the American Association of Anatomists

2020 Volume 250, Issue 2, Page(s) 134–144

Abstract: Background: Fibroblast Growth Factor 20 (FGF20)-FGF receptor 1 (FGFR1) signaling is essential for cochlear hair cell (HC) and supporting cell (SC) differentiation. In other organ systems, FGFR1 signals through several intracellular pathways including ... ...

Abstract	Background: Fibroblast Growth Factor 20 (FGF20)-FGF receptor 1 (FGFR1) signaling is essential for cochlear hair cell (HC) and supporting cell (SC) differentiation. In other organ systems, FGFR1 signals through several intracellular pathways including MAPK (ERK), PI3K, phospholipase C ɣ (PLCɣ), and p38. Previous studies implicated MAPK and PI3K pathways in HC and SC development. We hypothesized that one or both would be important downstream mediators of FGF20-FGFR1 signaling for HC differentiation. Results: By inhibiting pathways downstream of FGFR1 in cochlea explant cultures, we established that both MAPK and PI3K pathways are required for HC differentiation while PLCɣ and p38 pathways are not. Examining the canonical PI3K pathway, we found that while AKT is necessary for HC differentiation, it is not sufficient to rescue the Fgf20 Conclusions: Together, these data provide evidence that both MAPK and PI3K are important downstream mediators of FGF20-FGFR1 signaling during HC and SC differentiation.
MeSH term(s)	Animals ; Cell Differentiation ; Female ; Fibroblast Growth Factor 9 ; Fibroblast Growth Factors/metabolism ; MAP Kinase Signaling System ; Male ; Mice, Inbred C57BL ; Mice, Knockout ; Organ Culture Techniques ; Organ of Corti/cytology ; Organ of Corti/growth & development ; Organ of Corti/metabolism ; PTEN Phosphohydrolase/antagonists & inhibitors ; Phosphatidylinositol 3-Kinases/metabolism ; Phospholipase C gamma/metabolism ; Proto-Oncogene Proteins c-akt/metabolism ; Receptor, Fibroblast Growth Factor, Type 1/metabolism ; p38 Mitogen-Activated Protein Kinases/metabolism ; Mice
Chemical Substances	Fgf20 protein, mouse ; Fibroblast Growth Factor 9 ; Fibroblast Growth Factors (62031-54-3) ; Fgfr1 protein, mouse (EC 2.7.10.1) ; Receptor, Fibroblast Growth Factor, Type 1 (EC 2.7.10.1) ; Proto-Oncogene Proteins c-akt (EC 2.7.11.1) ; p38 Mitogen-Activated Protein Kinases (EC 2.7.11.24) ; PTEN Phosphohydrolase (EC 3.1.3.67) ; Phospholipase C gamma (EC 3.1.4.3)
Language	English
Publishing date	2020-09-09
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	1102541-4
ISSN	1097-0177 ; 1058-8388
ISSN (online)	1097-0177
ISSN	1058-8388
DOI	10.1002/dvdy.231
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Article: Fibroblast growth factor receptor signaling in cardiomyocytes is protective in the acute phase following ischemia-reperfusion injury.

Matsiukevich, Dzmitry / House, Stacey L / Weinheimer, Carla / Kovacs, Attila / Ornitz, David M

Frontiers in cardiovascular medicine

2022 Volume 9, Page(s) 1011167

Abstract: Fibroblast growth factor receptors (FGFRs) are expressed in multiple cell types in the adult heart. Previous studies have shown a cardioprotective effect of some FGF ligands in cardiac ischemia-reperfusion (I/R) injury and a protective role for ... ...

Abstract	Fibroblast growth factor receptors (FGFRs) are expressed in multiple cell types in the adult heart. Previous studies have shown a cardioprotective effect of some FGF ligands in cardiac ischemia-reperfusion (I/R) injury and a protective role for endothelial FGFRs in post-ischemic vascular remodeling. To determine the direct role FGFR signaling in cardiomyocytes in acute cardiac I/R injury, we inactivated
Language	English
Publishing date	2022-09-23
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2781496-8
ISSN	2297-055X
ISSN	2297-055X
DOI	10.3389/fcvm.2022.1011167
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Article ; Online: Loss of Fgf9 in mice leads to pancreatic hypoplasia and asplenia.

Patzek, Sophie / Liu, Zhe / de la O, Sean / Chang, Sean / Byrnes, Lauren E / Zhang, Xiuqin / Ornitz, David M / Sneddon, Julie B

iScience

2023 Volume 26, Issue 4, Page(s) 106500

Abstract: Pancreatic development requires spatially and temporally controlled expression of growth factors derived from mesenchyme. Here, we report that in mice the secreted factor Fgf9 is expressed principally by mesenchyme and then mesothelium during early ... ...

Abstract	Pancreatic development requires spatially and temporally controlled expression of growth factors derived from mesenchyme. Here, we report that in mice the secreted factor Fgf9 is expressed principally by mesenchyme and then mesothelium during early development, then subsequently by both mesothelium and rare epithelial cells by E12.5 and onwards. Global knockout of the
Language	English
Publishing date	2023-03-25
Publishing country	United States
Document type	Journal Article
ISSN	2589-0042
ISSN (online)	2589-0042
DOI	10.1016/j.isci.2023.106500
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