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Article ; Online: Bone morphogenetic protein signaling: the pathway and its regulation.

Akiyama, Takuya / Raftery, Laurel A / Wharton, Kristi A

2023 Volume 226, Issue 2

Abstract: In the mid-1960s, bone morphogenetic proteins (BMPs) were first identified in the extracts of bone to have the remarkable ability to induce heterotopic bone. When the Drosophila gene decapentaplegic (dpp) was first identified to share sequence similarity ...

Abstract	In the mid-1960s, bone morphogenetic proteins (BMPs) were first identified in the extracts of bone to have the remarkable ability to induce heterotopic bone. When the Drosophila gene decapentaplegic (dpp) was first identified to share sequence similarity with mammalian BMP2/BMP4 in the late-1980s, it became clear that secreted BMP ligands can mediate processes other than bone formation. Following this discovery, collaborative efforts between Drosophila geneticists and mammalian biochemists made use of the strengths of their respective model systems to identify BMP signaling components and delineate the pathway. The ability to conduct genetic modifier screens in Drosophila with relative ease was critical in identifying the intracellular signal transducers for BMP signaling and the related transforming growth factor-beta/activin signaling pathway. Such screens also revealed a host of genes that encode other core signaling components and regulators of the pathway. In this review, we provide a historical account of this exciting time of gene discovery and discuss how the field has advanced over the past 30 years. We have learned that while the core BMP pathway is quite simple, composed of 3 components (ligand, receptor, and signal transducer), behind the versatility of this pathway lies multiple layers of regulation that ensures precise tissue-specific signaling output. We provide a sampling of these discoveries and highlight many questions that remain to be answered to fully understand the complexity of BMP signaling.
MeSH term(s)	Animals ; Bone Morphogenetic Proteins/metabolism ; Drosophila/genetics ; Drosophila Proteins/genetics ; Gene Expression Regulation, Developmental ; Mammals/genetics ; Signal Transduction/physiology ; Transforming Growth Factor beta/metabolism
Chemical Substances	Bone Morphogenetic Proteins ; dpp protein, Drosophila ; Drosophila Proteins ; Transforming Growth Factor beta
Language	English
Publishing date	2023-12-20
Publishing country	United States
Document type	Review ; Journal Article
ZDB-ID	2167-2
ISSN	1943-2631 ; 0016-6731
ISSN (online)	1943-2631
ISSN	0016-6731
DOI	10.1093/genetics/iyad200
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Article ; Online: BMP/TGF-β signaling as a modulator of neurodegeneration in ALS.

Russo, Kathryn / Wharton, Kristi A

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

2021 Volume 251, Issue 1, Page(s) 10–25

Abstract: This commentary focuses on the emerging intersection between BMP/TGF-β signaling roles in nervous system function and the amyotrophic lateral sclerosis (ALS) disease state. Future research is critical to elucidate the molecular underpinnings of this ... ...

Abstract	This commentary focuses on the emerging intersection between BMP/TGF-β signaling roles in nervous system function and the amyotrophic lateral sclerosis (ALS) disease state. Future research is critical to elucidate the molecular underpinnings of this intersection of the cellular processes disrupted in ALS and those influenced by BMP/TGF-β signaling, including synapse structure, neurotransmission, plasticity, and neuroinflammation. Such knowledge promises to inform us of ideal entry points for the targeted modulation of dysfunctional cellular processes in an effort to abrogate ALS pathologies. It is likely that different interventions are required, either at discrete points in disease progression, or across multiple dysfunctional processes which together lead to motor neuron degeneration and death. We discuss the challenging, but intriguing idea that modulation of the pleiotropic nature of BMP/TGF-β signaling could be advantageous, as a way to simultaneously treat defects in more than one cell process across different forms of ALS.
MeSH term(s)	Amyotrophic Lateral Sclerosis/pathology ; Disease Progression ; Humans ; Transforming Growth Factor beta
Chemical Substances	Transforming Growth Factor beta
Language	English
Publishing date	2021-03-29
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1102541-4
ISSN	1097-0177 ; 1058-8388
ISSN (online)	1097-0177
ISSN	1058-8388
DOI	10.1002/dvdy.333
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Article ; Online: William Martin Gelbart 1945-2015.

Wharton, Kristi

Nature genetics

2015 Volume 47, Issue 12, Page(s) 1372

MeSH term(s)	Awards and Prizes ; Biomedical Research ; Genetics/history ; Genomics/history ; History, 20th Century ; History, 21st Century ; Humans
Language	English
Publishing date	2015-12
Publishing country	United States
Document type	Biography ; Historical Article ; Journal Article
ZDB-ID	1108734-1
ISSN	1546-1718 ; 1061-4036
ISSN (online)	1546-1718
ISSN	1061-4036
DOI	10.1038/ng.3455
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Article ; Online: Heterodimerization-dependent secretion of bone morphogenetic proteins in Drosophila.

Bauer, Milena / Aguilar, Gustavo / Wharton, Kristi A / Matsuda, Shinya / Affolter, Markus

Developmental cell

2023 Volume 58, Issue 8, Page(s) 645–659.e4

Abstract: Combinatorial signaling is key to instruct context-dependent cell behaviors. During embryonic development, adult homeostasis, and disease, bone morphogenetic proteins (BMPs) act as dimers to instruct specific cellular responses. BMP ligands can form both ...

Abstract	Combinatorial signaling is key to instruct context-dependent cell behaviors. During embryonic development, adult homeostasis, and disease, bone morphogenetic proteins (BMPs) act as dimers to instruct specific cellular responses. BMP ligands can form both homodimers or heterodimers; however, obtaining direct evidence of the endogenous localization and function of each form has proven challenging. Here, we make use of precise genome editing and direct protein manipulation via protein binders to dissect the existence and functional relevance of BMP homodimers and heterodimers in the Drosophila wing imaginal disc. This approach identified in situ the existence of Dpp (BMP2/4)/Gbb (BMP5/6/7/8) heterodimers. We found that Gbb is secreted in a Dpp-dependent manner in the wing imaginal disc. Dpp and Gbb form a gradient of heterodimers, whereas neither Dpp nor Gbb homodimers are evident under endogenous physiological conditions. We find that the formation of heterodimers is critical for obtaining optimal signaling and long-range BMP distribution.
MeSH term(s)	Animals ; Drosophila ; Drosophila Proteins/metabolism ; Bone Morphogenetic Proteins/metabolism ; Signal Transduction/physiology ; Ligands ; Wings, Animal/metabolism ; Drosophila melanogaster/genetics ; Drosophila melanogaster/metabolism
Chemical Substances	Drosophila Proteins ; Bone Morphogenetic Proteins ; Ligands ; dpp protein, Drosophila
Language	English
Publishing date	2023-04-12
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; 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.2023.03.008
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Article ; Online: Dogs (Canis familiaris) prioritize independent exploration over looking back.

Johnston, Angie M / Chang, Linda W / Wharton, Kristi / Santos, Laurie R

Journal of comparative psychology (Washington, D.C. : 1983)

2021 Volume 135, Issue 3, Page(s) 370–381

Abstract: It has been suggested that over the course of domestication, dogs developed the propensity to "look back" or gaze at humans when they encounter a challenging task. Unfortunately, little work to date has addressed the question of why dogs look back. To ... ...

Abstract	It has been suggested that over the course of domestication, dogs developed the propensity to "look back" or gaze at humans when they encounter a challenging task. Unfortunately, little work to date has addressed the question of why dogs look back. To explore this issue, we conducted 3 experiments in which dogs had the option of doing something other than looking back at their owner when encountering an unsolvable task. In Experiments 1 and 2, dogs could look back or attempt an alternative puzzle. In both experiments, dogs attempted the alternative puzzle prior to looking back. In Experiment 3, when dogs encountered the unsolvable task, they could look back or attempt to solve the same puzzle using an alternate approach. As in Experiments 1 and 2, dogs attempted the alternate approach prior to looking back. Although some scholars have suggested that dogs may look back because they are overly reliant on humans, our findings suggest that dogs may instead prioritize independent exploration over looking back. (PsycInfo Database Record (c) 2021 APA, all rights reserved).
MeSH term(s)	Animals ; Behavior, Animal ; Dogs ; Domestication ; Wolves
Language	English
Publishing date	2021-09-22
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	3130-6
ISSN	1939-2087 ; 0735-7036 ; 0093-4127
ISSN (online)	1939-2087
ISSN	0735-7036 ; 0093-4127
DOI	10.1037/com0000233
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Article ; Online: Alternative cleavage of the bone morphogenetic protein (BMP), Gbb, produces ligands with distinct developmental functions and receptor preferences.

Anderson, Edward N / Wharton, Kristi A

The Journal of biological chemistry

2017 Volume 292, Issue 47, Page(s) 19160–19178

Abstract: The family of TGF-β and bone morphogenetic protein (BMP) signaling proteins has numerous developmental and physiological roles. They are made as proprotein dimers and then cleaved by proprotein convertases to release the C-terminal domain as an active ... ...

Abstract	The family of TGF-β and bone morphogenetic protein (BMP) signaling proteins has numerous developmental and physiological roles. They are made as proprotein dimers and then cleaved by proprotein convertases to release the C-terminal domain as an active ligand dimer. Multiple proteolytic processing sites in Glass bottom boat (Gbb), the
MeSH term(s)	Activin Receptors, Type II/genetics ; Activin Receptors, Type II/metabolism ; Animals ; Body Patterning/physiology ; Cells, Cultured ; Drosophila Proteins/genetics ; Drosophila Proteins/metabolism ; Drosophila melanogaster/genetics ; Drosophila melanogaster/growth & development ; Drosophila melanogaster/metabolism ; Gene Expression Regulation, Developmental ; Ligands ; Proprotein Convertases/metabolism ; Pupa/genetics ; Pupa/growth & development ; Pupa/metabolism ; Receptors, Cell Surface/genetics ; Receptors, Cell Surface/metabolism ; Signal Transduction ; Transforming Growth Factor beta/genetics ; Transforming Growth Factor beta/metabolism ; Wings, Animal/growth & development ; Wings, Animal/metabolism
Chemical Substances	Drosophila Proteins ; Ligands ; Receptors, Cell Surface ; Transforming Growth Factor beta ; gbb protein, Drosophila ; wit protein, Drosophila ; Activin Receptors, Type II (EC 2.7.11.30) ; put protein, Drosophila (EC 2.7.11.30) ; Proprotein Convertases (EC 3.4.21.-)
Language	English
Publishing date	2017-09-18
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2997-x
ISSN	1083-351X ; 0021-9258
ISSN (online)	1083-351X
ISSN	0021-9258
DOI	10.1074/jbc.M117.793513
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Article ; Online: Corrigendum to "JAK/STAT signaling prevents excessive apoptosis to ensure maintenance of the interfollicular stalk critical for Drosophila oogenesis" [Dev. Biol. 438 (2018) 1-9].

Borensztejn, Antoine / Mascaro, Alexandra / Wharton, Kristi A

Developmental biology

2018 Volume 444, Issue 1, Page(s) 41

Language	English
Publishing date	2018-10-09
Publishing country	United States
Document type	Journal Article ; Published Erratum
ZDB-ID	1114-9
ISSN	1095-564X ; 0012-1606
ISSN (online)	1095-564X
ISSN	0012-1606
DOI	10.1016/j.ydbio.2018.09.020
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Article ; Online: JAK/STAT signaling prevents excessive apoptosis to ensure maintenance of the interfollicular stalk critical for Drosophila oogenesis.

Borensztejn, Antoine / Mascaro, Alexandra / Wharton, Kristi A

Developmental biology

2018 Volume 438, Issue 1, Page(s) 1–9

Abstract: Apoptosis not only eliminates cells that are damaged or dangerous but also cells whose function during development in patterning or organogenesis is complete. The successful formation of germ cells is essential for the perpetuation of a species. The ... ...

Abstract	Apoptosis not only eliminates cells that are damaged or dangerous but also cells whose function during development in patterning or organogenesis is complete. The successful formation of germ cells is essential for the perpetuation of a species. The production of an oocyte often depends on signaling between germline and somatic cells, but also between specialized types of somatic cells. In Drosophila, each developing egg chamber is separated from the next by a single file of interfollicular somatic cells. Little is known about the function of the interfollicular stalk, although its presumed role in separating egg chambers is to ensure that patterning cues from one egg chamber do not impact or disrupt the development of adjacent egg chambers. We found that cells comprising the stalk undergo a progressive decrease in number during oogenesis through an apoptotic-dependent loss. The extent of programmed cell death is restricted by JAK/STAT signaling in a cell-autonomous manner to ensure that the stalk is maintained. Both a failure to undergo the normal reduction in stalk cell number, or to prevent excessive stalk cell apoptosis results in a decrease in fecundity. Thus, activation of JAK/STAT signaling in the Drosophila interfollicular stalk emerges as a model to study the tight regulation of signaling-dependent apoptosis.
MeSH term(s)	Animals ; Apoptosis/genetics ; Cell Count ; Drosophila/metabolism ; Drosophila Proteins/metabolism ; Female ; Immunohistochemistry ; Janus Kinases/metabolism ; Oogenesis/genetics ; Oogenesis/physiology ; Ovarian Follicle/cytology ; Ovarian Follicle/physiology ; Ovary/cytology ; Ovary/metabolism ; Ovary/physiology ; STAT Transcription Factors/metabolism ; Signal Transduction/physiology
Chemical Substances	Drosophila Proteins ; STAT Transcription Factors ; Janus Kinases (EC 2.7.10.2)
Language	English
Publishing date	2018-03-21
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	1114-9
ISSN	1095-564X ; 0012-1606
ISSN (online)	1095-564X
ISSN	0012-1606
DOI	10.1016/j.ydbio.2018.03.018
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Article ; Online: Polypeptide Substrate Accessibility Hypothesis: Gain-of-Function R206H Mutation Allosterically Affects Activin Receptor-like Protein Kinase Activity.

Groppe, Jay C / Lu, Guorong / Tandang-Silvas, Mary R / Pathi, Anupama / Konda, Shruti / Wu, Jingfeng / Le, Viet Q / Culbert, Andria L / Shore, Eileen M / Wharton, Kristi A / Kaplan, Frederick S

Biomolecules

2023 Volume 13, Issue 7

Abstract: Although structurally similar to type II counterparts, type I or activin receptor-like kinases (ALKs) are set apart by a metastable helix-loop-helix (HLH) element preceding the protein kinase domain that, according to a longstanding paradigm, serves ... ...

Abstract	Although structurally similar to type II counterparts, type I or activin receptor-like kinases (ALKs) are set apart by a metastable helix-loop-helix (HLH) element preceding the protein kinase domain that, according to a longstanding paradigm, serves passive albeit critical roles as an inhibitor-to-substrate-binding switch. A single recurrent mutation in the codon of the penultimate residue, directly adjacent the position of a constitutively activating substitution, causes milder activation of ACVR1/ALK2 leading to sporadic heterotopic bone deposition in patients presenting with fibrodysplasia ossificans progressiva, or FOP. To determine the protein structural-functional basis for the gain of function, R206H mutant, Q207D (aspartate-substituted caALK2) and HLH subdomain-truncated (208 Ntrunc) forms were compared to one another and the wild-type enzyme through in vitro kinase and protein-protein interaction analyses that were complemented by signaling read-out (p-Smad) in primary mouse embryonic fibroblasts and
MeSH term(s)	Animals ; Mice ; Activin Receptors/genetics ; Gain of Function Mutation ; Activin Receptors, Type I/genetics ; Activin Receptors, Type I/metabolism ; Fibroblasts/metabolism ; Mutation ; Peptides/genetics
Chemical Substances	Activin Receptors (EC 2.7.11.30) ; Activin Receptors, Type I (EC 2.7.11.30) ; Peptides
Language	English
Publishing date	2023-07-14
Publishing country	Switzerland
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2701262-1
ISSN	2218-273X ; 2218-273X
ISSN (online)	2218-273X
ISSN	2218-273X
DOI	10.3390/biom13071129
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Article ; Online: Circuit Dysfunction in

Held, Aaron / Major, Paxton / Sahin, Asli / Reenan, Robert A / Lipscombe, Diane / Wharton, Kristi A

The Journal of neuroscience : the official journal of the Society for Neuroscience

2019 Volume 39, Issue 12, Page(s) 2347–2364

Abstract: Amyotrophic lateral sclerosis (ALS) is a devastating neurodegenerative disease for which the origin and underlying cellular defects are not fully understood. Although motor neuron degeneration is the signature feature of ALS, it is not clear whether ... ...

Abstract	Amyotrophic lateral sclerosis (ALS) is a devastating neurodegenerative disease for which the origin and underlying cellular defects are not fully understood. Although motor neuron degeneration is the signature feature of ALS, it is not clear whether motor neurons or other cells of the motor circuit are the site of disease initiation. To better understand the contribution of multiple cell types in ALS, we made use of a
MeSH term(s)	Amyotrophic Lateral Sclerosis/metabolism ; Animals ; Animals, Genetically Modified ; Bone Morphogenetic Proteins/metabolism ; Disease Models, Animal ; Drosophila ; Drosophila Proteins/genetics ; Feedback, Sensory/physiology ; Female ; Gene Knock-In Techniques ; Locomotion ; Male ; Motor Neurons/metabolism ; Nerve Degeneration/metabolism ; Proprioception/physiology ; Signal Transduction ; Superoxide Dismutase/genetics
Chemical Substances	Bone Morphogenetic Proteins ; Drosophila Proteins ; Sod1 protein, Drosophila (EC 1.15.1.1) ; Superoxide Dismutase (EC 1.15.1.1)
Language	English
Publishing date	2019-01-18
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	604637-x
ISSN	1529-2401 ; 0270-6474
ISSN (online)	1529-2401
ISSN	0270-6474
DOI	10.1523/JNEUROSCI.1771-18.2019
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