Patterning a complex organ: branching morphogenesis and nephron segmentation in kidney development.

doi:10.1016/J.DEVCEL.2010.04.008

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Patterning a complex organ: branching morphogenesis and nephron segmentation in kidney development.

Journal Article•DOI•

Patterning a complex organ: branching morphogenesis and nephron segmentation in kidney development.

Frank Costantini¹, Raphael Kopan²•Institutions (2)

Columbia University Medical Center¹, Washington University in St. Louis²

18 May 2010-Developmental Cell (NIH Public Access)-Vol. 18, Iss: 5, pp 698-712

TL;DR: The two major components of the kidney, the collecting system and the nephron, have different developmental histories, and their embryological origin and the genes controlling their morphogenesis, patterning, and differentiation are considered.

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About: This article is published in Developmental Cell.The article was published on 2010-05-18 and is currently open access. It has received 624 citations till now. The article focuses on the topics: Kidney development.

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Journal Article•DOI•

Redefining the In Vivo Origin of Metanephric Nephron Progenitors Enables Generation of Complex Kidney Structures from Pluripotent Stem Cells

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Atsuhiro Taguchi¹, Yusuke Kaku¹, Tomoko Ohmori¹, Sazia Sharmin¹, Minetaro Ogawa¹, Hiroshi Sasaki¹, Ryuichi Nishinakamura¹ - Show less +3 more•Institutions (1)

Kumamoto University¹

02 Jan 2014-Cell Stem Cell

TL;DR: By reevaluating the developmental origins of metanephric progenitors, this work has provided key insights into kidney specification in vivo and taken important steps toward kidney organogenesis in vitro.

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679 citations

Cites background from "Patterning a complex organ: branchi..."

...…the MM and ureteric bud lineage segregate from one another have not been clarified, despite many reports showing the importance of various growth factors during kidney development (Costantini and Kopan, 2010; Fleming et al., 2013; Kim and Dressler, 2005; Moriya et al., 1993; Poladia et al., 2006)....
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...However, the mechanisms underlying how the nascent mesoderm becomes committed to the intermediate mesoderm and how the MM and ureteric bud lineage segregate from one another have not been clarified, despite many reports showing the importance of various growth factors during kidney development (Costantini and Kopan, 2010; Fleming et al., 2013; Kim and Dressler, 2005; Moriya et al., 1993; Poladia et al., 2006)....
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Journal Article•DOI•

The front and rear of collective cell migration

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Roberto Mayor¹, Sandrine Etienne-Manneville²•Institutions (2)

University College London¹, Pasteur Institute²

01 Feb 2016-Nature Reviews Molecular Cell Biology

TL;DR: The recent studies have described how leader cells at the front of cell groups drive migration and have highlighted the importance of follower cells and cell-cell communication, both between followers and between follower and leader cells, to improve the efficiency of collective movement.

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Abstract: Collective cell migration has a key role during morphogenesis and during wound healing and tissue renewal in the adult, and it is involved in cancer spreading. In addition to displaying a coordinated migratory behaviour, collectively migrating cells move more efficiently than if they migrated separately, which indicates that a cellular interplay occurs during collective cell migration. In recent years, evidence has accumulated confirming the importance of such intercellular communication and exploring the molecular mechanisms involved. These mechanisms are based both on direct physical interactions, which coordinate the cellular responses, and on the collective cell behaviour that generates an optimal environment for efficient directed migration. The recent studies have described how leader cells at the front of cell groups drive migration and have highlighted the importance of follower cells and cell-cell communication, both between followers and between follower and leader cells, to improve the efficiency of collective movement.

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641 citations

Journal Article•DOI•

Identification of a potential mechanism of acute kidney injury during the COVID-19 outbreak: a study based on single-cell transcriptome analysis.

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Xiu wu Pan¹, Da Xu¹, Hao Zhang¹, Wang Zhou¹, Lin hui Wang¹, Xin gang Cui¹ - Show less +2 more•Institutions (1)

Second Military Medical University¹

31 Mar 2020-Intensive Care Medicine

TL;DR: The aim of this work is to contribute towards the humanizing of Urology and its role in medicine by providing a systematic literature review and meta-analysis of current treatments and experimental results.

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Abstract: Da Xu , Hao Zhang , Hai-yi Gong , Jia-xin Chen, Jian-qing Ye, Tong Meng , Si-shun Gan, Fa-jun Qu, Chuan-min Chu, Wang Zhou *, Xiu-wu Pan*, Lin-hui Wang*, Xin-gang Cui * Department of Urology, The Gongli Hospital of Second Military Medical University, 200135 Shanghai, China Depanrtment of Urology, The Third Affiliated Hospital of Second Military Medical University, 201805 Shanghai, China Department of Urology, The Changzheng Hospital of Second Military Medical University, 200003 Shanghai, China Peking-Tsinghua Center for Life Sciences, TsinghuaUniversity, 100084 Beijing, China Department of Bone Tumor Surgery, The Changzheng Hospital of Second Military Medical University, 200003 Shanghai, China Tongji University Cancer Center, School of Medicine, Tongji University, 200092 Shanghai, China Division of Spine, Department of Orthopedics, Tongji Hospital affiliated to Tongji University School of Medicine, 200065 Shanghai, China Qiu-Jiang Bioinformatics Institute, 200003 Shanghai, China These authors contributed equally to this work, and all should be considered first author *Correspondence to: cuixingang@smmu.edu.cn (Xin-gang Cui) wanglinhui@smmu.edu.cn (Lin-hui Wang) panxiuwu@126.com (Xiu-wu Pan) brilliant212@163.com (Wang Zhou) Preprints (www.preprints.org) | NOT PEER-REVIEWED | Posted: 23 February 2020

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431 citations

Cites background from "Patterning a complex organ: branchi..."

...differentiates into the metanephrogenic blastema and sequentially differentiates into proximal tubules, loop of henle, and distal tubules[21]....
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Journal Article•DOI•

Mammalian Kidney Development: Principles, Progress, and Projections

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Melissa H. Little¹, Andrew P. McMahon•Institutions (1)

University of Queensland¹

01 May 2012-Cold Spring Harbor Perspectives in Biology

TL;DR: Recent insights into central regulatory processes governing organ assembly and renal disease are focused on, and future directions for the field are predicted.

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Abstract: The mammalian kidney is a vital organ with considerable cellular complexity and functional diversity. Kidney development is notable for requiring distinct but coincident tubulogenic processes involving reciprocal inductive signals between mesenchymal and epithelial progenitor compartments. Key molecular pathways mediating these interactions have been identified. Further, advances in the analysis of gene expression and gene activity, coupled with a detailed knowledge of cell origins, are enhancing our understanding of kidney morphogenesis and unraveling the normal processes of postnatal repair and identifying disease-causing mechanisms. This article focuses on recent insights into central regulatory processes governing organ assembly and renal disease, and predicts future directions for the field.

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405 citations

Journal Article•DOI•

Comparative Analysis and Refinement of Human PSC-Derived Kidney Organoid Differentiation with Single-Cell Transcriptomics

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Haojia Wu¹, Kohei Uchimura¹, Erinn L. Donnelly¹, Yuhei Kirita¹, Samantha A. Morris¹, Benjamin D. Humphreys¹ - Show less +2 more•Institutions (1)

Washington University in St. Louis¹

06 Dec 2018-Cell Stem Cell

TL;DR: Brain-derived neurotrophic factor and its cognate receptor NTRK2 were expressed in the neuronal lineage during organoid differentiation, andhibiting this pathway improved organoid formation by reducing neurons by 90% without affecting kidney differentiation, highlighting the power of single-cell technologies to characterize and improve organoids differentiation.

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392 citations

Cites background from "Patterning a complex organ: branchi..."

...The ureteric bud undergoes branching morphogenesis to form the collecting system and is required for the formation of an interconnected collecting duct (Costantini and Kopan, 2010)....
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References

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Open Access

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Journal Article•DOI•

BMP-7 is an inducer of nephrogenesis, and is also required for eye development and skeletal patterning.

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Guangbin Luo¹, C. Hofmann¹, A. L. J. J. Bronckers¹, M. Sohocki¹, Allan Bradley¹, Gerard Karsenty¹ - Show less +2 more•Institutions (1)

University of Texas MD Anderson Cancer Center¹

15 Nov 1995-Genes & Development

TL;DR: In situ hybridization analysis showed that the absence of BMP-7 affects the expression of molecular markers of nephrogenesis, such as Pax-2 and Wnt-4 between 12.5 and 14.5 days postcoitum (dpc), which identifies B MP-7 as an inducer of neephrogenesis.

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Abstract: Bone morphogenetic proteins (BMPs) are multifunctional growth factors originally identified by their ability to induce ectopic bone formation. To investigate the function of one of the BMPs, BMP-7, we have generated BMP-7-deficient mice using embryonic stem cell technology. BMP-7-deficient mice die shortly after birth because of poor kidney development. Histological analysis of mutant embryos at several stages of development revealed that metanephric mesenchymal cells fail to differentiate, resulting in a virtual absence of glomerulus in newborn kidneys. In situ hybridization analysis showed that the absence of BMP-7 affects the expression of molecular markers of nephrogenesis, such as Pax-2 and Wnt-4 between 12.5 and 14.5 days postcoitum (dpc). This identifies BMP-7 as an inducer of nephrogenesis. In addition, BMP-7-deficient mice have eye defects that appear to originate during lens induction. Finally, BMP-7-deficient mice also have skeletal patterning defects restricted to the rib cage, the skull, and the hindlimbs.

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1,046 citations

"Patterning a complex organ: branchi..." refers background in this paper

...…requires autonomous expression of WT1 (Hartwig et al., 2010) and Sall1 (Nishinakamura and Osafune, 2006), the receptors FGFR1 and 2 (Poladia et al., 2006), and sources of FGF8 (Grieshammer et al., 2005; Perantoni et al., 2005) and BMP7 (Dudley et al., 1999; Kazama et al., 2008; Luo et al., 1995)....
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Book•

Organogenesis of the kidney

[...]

Lauri Saxén¹•Institutions (1)

University of Helsinki¹

01 Jan 1987

TL;DR: This study presents experimental methods to study kidney development through ontogenesis of the vertebrate excretory system and the role of tubulogenesis in kidney development.

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Abstract: This description of a model system for cell differentiation and organogenesis is written by one of the foremost researchers in the area. The main emphasis is on the mammalian kidney, but the book also deals with the development of the transien excretory organs. It includes discussions of induction, proliferation, early cytodifferentiation and morphogenesis and organogenesis. This authoritative account will be valuable to developmental biologists and also to scientists working in paediatric nephrology. As it gives the background of normal development and of control systems, it will also be of use to nephrologists working on abnormalities in the urinary tract.

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1,006 citations

"Patterning a complex organ: branchi..." refers background in this paper

...Cells in the dorsal IM coalesce into the nephric duct (ND, also called the Wolffian duct) (Saxen, 1987), while the mesenchymal cell population in the ventral IM, called the ‘‘nephrogenic cord,’’ remains undifferentiated (Figures 1 A–1C)....
[...]
...Polarity becomes apparent morphologically as the RV becomes the comma-shaped body; these stereotypical structures were so named because the first cells to elongate, change shape, and form a ‘‘slit’’ are located at the proximal end (Saxen, 1987)....
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...Nascent tubular structures normally appear beneath the UB tips, while the MM above the tips remains undifferentiated (Saxen, 1987)....
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Journal Article•DOI•

Pax-2 controls multiple steps of urogenital development

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Miguel Torres¹, Emilia Gómez-Pardo¹, Gregory R. Dressler¹, Peter Gruss¹•Institutions (1)

Max Planck Society¹

01 Dec 1995-Development

TL;DR: Pax-2 mouse mutants provide an animal model for human hereditary kidney diseases and data show that Pax-2 is required for multiple steps during the differentiation of intermediate mesoderm.

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Abstract: Urogenital system development in mammals requires the coordinated differentiation of two distinct tissues, the ductal epithelium and the nephrogenic mesenchyme, both derived from the intermediate mesoderm of the early embryo. The former give rise to the genital tracts, ureters and kidney collecting duct system, whereas mesenchymal components undergo epithelial transformation to form nephrons in both the mesonephric (embryonic) and metanephric (definitive) kidney. Pax-2 is a transcriptional regulator of the paired-box family and is widely expressed during the development of both ductal and mesenchymal components of the urogenital system. We report here that Pax-2 homozygous mutant newborn mice lack kidneys, ureters and genital tracts. We attribute these defects to dysgenesis of both ductal and mesenchymal components of the developing urogenital system. The Wolffian and Mullerian ducts, precursors of male and female genital tracts, respectively, develop only partially and degenerate during embryogenesis. The ureters, inducers of the metanephros are absent and therefore kidney development does not take place. Mesenchyme of the nephrogenic cord fails to undergo epithelial transformation and is not able to form tubules in the mesonephros. In addition, we show that the expression of specific markers for each of these components is de-regulated in Pax-2 mutants. These data show that Pax-2 is required for multiple steps during the differentiation of intermediate mesoderm. In addition, Pax-2 mouse mutants provide an animal model for human hereditary kidney diseases.

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860 citations

"Patterning a complex organ: branchi..." refers background in this paper

...Ectodermal signals are also required for the continued expression of Lhx1 and Pax2 in the ND, which in turn are important formaintenance of the epithelium (James and Schultheiss, 2005; Torres et al., 1995)....
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...Ectodermal signals are also required for the continued expression of Lhx1 and Pax2 in the ND, which in turn are important formaintenance of the epithelium (James and Schultheiss, 2005; Torres et al., 1995)....
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Journal Article•DOI•

Six2 Defines and Regulates a Multipotent Self-Renewing Nephron Progenitor Population throughout Mammalian Kidney Development

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Akio Kobayashi¹, M. Todd Valerius¹, Joshua W. Mugford¹, Thomas L. Carroll¹, Michelle Self, Guillermo Oliver², Andrew P. McMahon¹ - Show less +3 more•Institutions (2)

Harvard University¹, St. Jude Children's Research Hospital²

07 Aug 2008-Cell Stem Cell

TL;DR: Clonal analysis indicates that at least some Six2-expressing cells are multipotent, contributing to multiple domains of the nephron, and observations suggest that Six2 activity cell-autonomously regulates a multipotent nephrons progenitor population.

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850 citations

"Patterning a complex organ: branchi..." refers background or result in this paper

...Since mice that are simultaneously deficient for both Six2 andWnt9b cannot undergoMET (Kobayashi et al., 2008), Six2 activity in cells within the capping mesenchyme most likely blocks MET by antagonizing the b-catenin stabilizing effects of Wnt9b and thus maintaining the progenitor cell population…...
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...Chimera analysis indicated that although Six2"/" cells could contribute to all cell fates within the nephron, they could not self-renew (Kobayashi et al., 2008)....
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...…mesenchyme most likely blocks MET by antagonizing the b-catenin stabilizing effects of Wnt9b and thus maintaining the progenitor cell population (Carroll et al., 2005; Kispert et al., 1998; Kobayashi et al., 2008; Kuure et al., 2007; Majumdar et al., 2003; Park et al., 2007; Self et al., 2006)....
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...This is consistent with Six2/Cited expression marking the committed progenitor pool of the renal epithelium (Boyle et al., 2008; Kobayashi et al., 2008)....
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...Importantly, fate mapping confirms that, like Six2"/" cells, Wnt4"/" cells can only contribute to the RV and its subsequent structures but can no longer contribute to the progenitor pool (Kobayashi et al., 2008; Shan et al., 2009)....
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Journal Article•DOI•

Wnt9b plays a central role in the regulation of mesenchymal to epithelial transitions underlying organogenesis of the mammalian urogenital system.

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Thomas L. Carroll¹, Joo-Seop Park¹, Shigemi Hayashi², Shigemi Hayashi¹, Arindam Majumdar³, Arindam Majumdar¹, Andrew P. McMahon¹ - Show less +3 more•Institutions (3)

Harvard University¹, Novartis², Karolinska Institutet³

01 Aug 2005-Developmental Cell

TL;DR: It is shown that Wnt9b is expressed in the inductive epithelia and is essential for the development of mesonephric and metanephric tubules and caudal extension of the Müllerian duct, and this data implicate canonical Wnt signaling as one of the major pathways in the organization of the mammalian urogenital system.

...read moreread less

807 citations

"Patterning a complex organ: branchi..." refers background in this paper

...As noted above, after the Six2-expressing MM cells extinguish Cited1, they begin to stabilize b-catenin in response to Wnt9b, which can instruct MM cells to undergo MET....
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...Mice 706 Developmental Cell 18, May 18, 2010 ª2010 Elsevier Inc. deficient in Wnt9b fail to undergo MET (Carroll et al., 2005), whereas mice deficient in Six2 undergo exuberant MET: they form renal vesicle (RV)-like epithelial aggregates above and below the UB branches (Figure 4E) (Self et al., 2006)....
[...]
...Expression of MET is important for the ability of HGF to regulate UB branching (Liu et al., 2009)....
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...…mesenchyme most likely blocks MET by antagonizing the b-catenin stabilizing effects of Wnt9b and thus maintaining the progenitor cell population (Carroll et al., 2005; Kispert et al., 1998; Kobayashi et al., 2008; Kuure et al., 2007; Majumdar et al., 2003; Park et al., 2007; Self et al., 2006)....
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...…Wnt9b are not interchangeable: both factors are capable of inducing RV formation and tubulogenesis in isolated MM, but Wnt9b-expressing cells cannot induce differentiation in Wnt4"/" MM, whereas Wnt4 can induce RV formation and tubulogenesis in competent Wnt9b"/" mesenchyme (Carroll et al., 2005)....
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