Development of the definitive kidney in the cynomolgus monkey (<i>Macaca fascicularis</i>)

Rodriguez, C. G.; Makori, Norbert; Cukierski, Mark A.; Hendrickx, Andrew G.

doi:10.1111/j.1600-0684.1996.tb00203.x

Cited by 9 publications

(6 citation statements)

References 19 publications

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“…PAX2 and Vimentin immunoreactivity shown in developing rhesus monkeys during kidney ontogeny is similar to findings in human specimens at similar gestational ages (Winyard, et al, 1996, Naruse et al, 2000) and further supports the importance of the monkey as a model for human nephrogenesis (Lee et al, 2001; Rodriguez et al, 1996). Similar to findings in humans and rodents, PAX2 is an important marker of kidney development in the monkey with strong expression at the ureteric bud tips, the condensed mesenchyme and renal vesicle, and in the developing visceral and parietal layers of the capsule.…”

Section: Discussionsupporting

confidence: 79%

“…Several studies have focused on kidney development, from early precursors to the events associated with the formation of the definitive or metanephric kidney (Burrow, 2000; Dressler, 2006; Rodriguez et al, 1996). The essential process for metanephric kidney formation is the reciprocal induction of the mesoderm-derived metanephric mesenchyme (blastema) and the branching ureteric bud (derived from the mesonephric duct), which forms the excretory component and collecting system of the kidney, respectively, and is under the control of key genes and their protein products (Saxen, 1987).…”

Section: Introductionmentioning

confidence: 99%

“…Developmental similarities include spatial and temporal pattern of organ development, placental structure, and growth characteristics, to name a few (Lee et al, 2001; Rodriguez et al, 1996; Tarantal, 2005; Tarantal and Gargosky, 1995; Tarantal et al, 2001). In these studies, rhesus monkey kidneys at sequential gestational ages were assessed by immunohistochemistry for the expression of renal developmental markers PAX2, an essential marker of kidney differentiation (Dressler, 1996), and Vimentin, a mesenchymal (Holthöfer et al, 1984; Naruse et al, 2000; Carev et al, 2008) and renal prognostic marker (Moll et al, 1991; Gonlusen et al, 2001), to provide additional insights relevant to hESC differentiation protocols.…”

Section: Introductionmentioning

confidence: 99%

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Renal ontogeny in the rhesus monkey (Macaca mulatta) and directed differentiation of human embryonic stem cells towards kidney precursors

et al. 2009

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The development of the metanephric kidney was studied immunohistochemically across gestation in monkeys to identify markers of cell specification, and to aid in developing experimental paradigms for renal precursor differentiation from human embryonic stem cells (hESC). PAX2, an important kidney developmental marker, was expressed at the tips of the ureteric bud, in the surrounding condensing mesenchyme, and in the renal vesicle. Vimentin, a mesenchymal and renal marker, was strongly expressed in the metanephric blastema then found to be limited to the glomerulus and interstitial cells of the medulla and cortex. A model of gene expression based on human and nonhuman primate renal ontogeny was developed and incorporated into studies of hESC differentiation. Spontaneous hESC differentiation revealed markers of metanephric mesenchyme (OSR1, PAX2, SIX2, WT1) that increased over time, followed by upregulation of kidney precursor markers (EYA1, LIM1, CD24). Directed hESC differentiation was also evaluated with the addition of Retinoic Acid, Activin-A, and BMP-4 or BMP-7, and using different culture substrate conditions. Of the culture substrates studied, gelatin most closely recapitulated the anticipated directed developmental pattern of renal gene expression. No differences were found when BMP-4 and BMP-7 were compared to baseline conditions. PAX2 and Vimentin immunoreactivity in differentiating hESC was also similar to the renal precursor patterns reported for human fetal kidneys and findings described in rhesus monkeys. The results of these studies: (1) provide additional data to support that rhesus monkey kidney development parallels that of humans, and (2) provide a useful model for hESC directed differentiation towards renal precursors.

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Section: Discussionsupporting

confidence: 79%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Renal ontogeny in the rhesus monkey (Macaca mulatta) and directed differentiation of human embryonic stem cells towards kidney precursors

et al. 2009

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“…Notably, obstructed kidneys also showed a severe disruption of normal glomerular development with consequent podocyte apoptosis and loss (9). This in utero monkey model of human obstructive renal dysplasia is particularly important since monkeys exhibit active nephrogenesis comparable to humans during similar developmental time periods, with a well-demarcated nephrogenic zone and identifiable metanephric mesenchyme, ureteric bud, S-shaped nephrons, and maturing glomeruli (10,11). Thus, the fetal rhesus monkey model can be instrumental in understanding the role of podocytes in the prenatal pathogenesis of obstructive renal dysplasia and for developing potential cell-based therapies using podocyte progenitors for human applications.…”

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confidence: 99%

Characterization and Culture of Fetal Rhesus Monkey Renal Cortical Cells

et al. 2009

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The renal glomerulus is composed of endothelial and mesangial cells with podocytes contributing to glomerular filtration. Podocyte damage is associated with renal disorders, thus there is interest in these cells for regenerative medicine. These studies investigated the use of extracellular matrix (ECM) to grow third trimester fetal monkey renal cortical cells and to assess mature podocytes in culture. Immunohistochemistry provided a profile of podocyte differentiation with metanephric mesenchyme and developing podocytes nestin positive and synaptopodin negative, whereas mature podocytes were positive for both markers. Primary cell cultures devoid of mature podocytes were established on plastic and renal ECM. A cell population (nestin+/synatopodin−) cultured on renal ECM showed greater proliferative potential compared to plastic with limited podocytes developing in culture over time. Further investigation of individual components of ECM (laminin, fibronectin, collagen I or IV) indicated that collagen I supported the greatest proliferation similar to renal ECM, whereas a greater number of mature podocytes (nestin+/synaptopodin+) were observed on fibronectin. These results suggest: (1) culture of fetal monkey podocytes can be accomplished, (2) renal ECM and collagen I can support renal cortical cells in vitro which may recapitulate the developing kidney in vivo, and (3) fibronectin can support podocyte differentiation in vitro.

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“…Although kidney development in humans and some nonhuman primates has been studied (22,23), the time course of nephrogenesis in the baboon remains unknown. For verifying the potential usefulness of the baboon as a model to study the effects of preterm delivery on kidney development, it is essential to determine the time course of nephrogenesis in the baboon and in particular whether nephrogenesis is complete at term.…”

mentioning

confidence: 99%

The Baboon as a Good Model for Studies of Human Kidney Development

Gubhaju

Black

2005

Pediatr Res

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Because of the improved survival of premature neonates in recent years, it is important to investigate the effects of premature delivery on the kidney, in which nephrogenesis is still ongoing during the third trimester. Hence, an appropriate animal model that is similar to humans is essential. The aim of the current study is to determine the time course of nephrogenesis in the baboon, to establish whether it is a suitable model of human nephrogenesis. At the Southwest Foundation for Biomedical Research (San Antonio, TX), fetal baboons were delivered prematurely by cesarean delivery and at term by natural delivery. Fixed kidneys from 125-, 140-, 175-, and 185-d gestation baboons were assessed morphologically for evidence of a nephrogenic zone. Nephron number, kidney volume, and glomerular and corpuscle volume were also estimated using unbiased stereology. Morphologic assessment confirmed the presence of metanephric mesenchyme and immature glomeruli in the nephrogenic zone of the kidneys from the prematurely delivered fetuses at 125 and 140 d gestation. At 175 d gestation and at term, the nephrons seemed to be mature. Both kidney weight (R 2 ϭ 0.918, p ϭ 0.0002) and kidney volume (R 2 ϭ 0.837, p ϭ 0.001) were very strongly correlated with nephron number. There was also a direct relationship between gestational age (R 2 ϭ 0.589, p ϭ 0.03) and birth weight (R 2 ϭ 0.562, p ϭ 0.03) with nephron number. In conclusion, in this study, nephrogenesis in the baboon is complete before term by 175 d gestation, which is similar to humans. Hence, the baboon is a suitable model for future studies to investigate human kidney development. The incidence of premature delivery has increased substantially in the past decade, such that 6 -10% of all births in the Western world are premature (1). Moreover, as a result of marked advances in neonatal care, infants who are born as early as 26 wk gestation currently have an 80% chance of survival (2). Therefore, it is imperative to understand how organ development is affected in prematurely delivered individuals, especially in organs in which the ontogeny normally occurs before birth. For instance, infant respiratory distress syndrome and bronchopulmonary dysplasia are commonly observed in preterm neonates as a result of the immaturity of the lungs as pulmonary development is ongoing until term in the human (3). However, in recent years, neonatologists have been able to overcome respiratory complications to some extent by enhancing postnatal lung development, thus increasing survival of premature infants.Renal development is also rapidly occurring during the third trimester of pregnancy, and so the kidney may also be "at risk" after premature delivery. Indeed, renal failure affects~8 -24% of all preterm neonates as a result of the immature kidneys (4).Nephrogenesis, the formation of nephrons, commences at approximately the ninth week of gestation and continues until 36 wk in humans (5,6); hence, it is probable that nephrogenesis is affected in infants who are born before 36 wk gestation. Ne...

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Development of the definitive kidney in the cynomolgus monkey (Macaca fascicularis)

Cited by 9 publications

References 19 publications

Renal ontogeny in the rhesus monkey (Macaca mulatta) and directed differentiation of human embryonic stem cells towards kidney precursors

Renal ontogeny in the rhesus monkey (Macaca mulatta) and directed differentiation of human embryonic stem cells towards kidney precursors

Characterization and Culture of Fetal Rhesus Monkey Renal Cortical Cells

The Baboon as a Good Model for Studies of Human Kidney Development

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