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Intermediate mesoderm

The intermediate mesoderm is a transient embryonic layer in vertebrates that arises during as a narrow strip of cells positioned between the paraxial mesoderm and the along the anteroposterior axis of the . It originates from epiblast cells that ingress through the posterior , influenced by signaling pathways such as , Nodal, and FGF, which specify its distinct identity separate from neighboring al lineages. This mesoderm is characterized by the expression of key transcription factors including Osr1, Pax2, and Lhx1, which regulate its patterning and . During early development, around the third week post-fertilization in humans or embryonic day 8 in mice, the intermediate mesoderm lies ventral to the somites and adjacent to the dorsal aorta, forming a bilateral cord that elongates and segments along the body axis. It undergoes anteroposterior patterning, with anterior regions giving rise to structures like the ureteric and posterior regions contributing to the metanephric , driven by gradients of morphogens such as and Wnt signaling. The intermediate mesoderm's primary derivatives include the urogenital system: it generates the kidneys through sequential formation of the pronephros (a transient structure that regresses in mammals), mesonephros (which functions temporarily and contributes to hematopoietic cells), and metanephros (the definitive formed via between the ureteric and metanephrogenic ). Additionally, it forms the gonads, , and associated ducts, such as the mesonephric (Wolffian) ducts in males and paramesonephric (Müllerian) ducts in females, essential for reproductive and excretory functions. Notable aspects of intermediate mesoderm development highlight its role in , involving complex epithelial-mesenchymal interactions and genes like Gdnf, Wt1, and Fgf2 that ensure proper and formation. Disruptions in its specification or differentiation can lead to congenital anomalies such as or disorders of sexual development, underscoring its clinical significance. Recent advances in biology have enabled the in vitro generation of intermediate mesoderm progenitors from pluripotent cells, facilitating studies of urogenital diseases and .

Embryonic Origin and Formation

Location and Initial Specification

The intermediate mesoderm constitutes a transient longitudinal strip of tissue positioned between the paraxial mesoderm, which forms the somites, and the in the early embryo. This narrow band emerges as a distinct domain during the initial stages of mesoderm diversification, serving as the progenitor population for urogenital structures without itself persisting as a mature tissue. Its formation occurs during , approximately weeks 3 to 4 of , when epiblast cells undergo epithelial-to-mesenchymal transition and ingress through the to populate the mesodermal layer. In this process, cells destined for the intermediate mesoderm migrate laterally from the streak, establishing its mediolateral position relative to other mesodermal subtypes. This ingression is temporally coordinated with the overall movements, ensuring the intermediate mesoderm aligns along the embryonic axis before further patterning. Spatial patterning of the intermediate mesoderm along the mediolateral axis is governed by opposing gradients of signaling molecules, including (BMPs) that promote lateral fates and (FGFs) that promote medial paraxial fates. These gradients interact with broader cues, such as those from adjacent tissues, to refine the boundaries between paraxial, intermediate, and lateral domains during early somitogenesis. This organizational principle is evolutionarily conserved across vertebrates, as demonstrated in model organisms like the and . In the , fate-mapping studies reveal that intermediate mesoderm precursors ingress through the mid- to posterior levels of the around embryonic day 6.5 to 7.5. Similarly, in the , cells fated to the intermediate mesoderm enter via specific primitive groove positions during stages 3 to 5 of Hamburger-Hamilton , highlighting the precision of streak-level allocation in establishing mediolateral identity.

Molecular Mechanisms of Induction

The specification of (IM) during vertebrate relies on inductive signals that establish a dorsoventral across the mesodermal sheet, positioned between the dorsal paraxial mesoderm and ventral . 4 (BMP4), secreted from the , acts in a dose-dependent manner to pattern mesoderm fates, with intermediate BMP4 levels promoting IM formation while higher levels specify and lower levels favor paraxial mesoderm. Concurrently, Vg1 and Nodal signals emanating from the underlying contribute to this , with Vg1/Nodal heterodimers inducing mesendodermal fates and specifically promoting IM at moderate intensities through activation of shared downstream effectors like Smad1/5/8, which integrate with BMP signaling. These opposing yet complementary gradients ensure precise IM commitment by balancing ventralizing BMP influences with dorsalizing Nodal inputs during early . Around the 6-somite stage in and embryos, IM-specific genes are activated in a narrow stripe lateral to the somites, marking the initial commitment to this lineage. Key markers such as Pax2 and initiate expression at this stage, delineating the IM domain, while Lhx1 (also known as Lim1) becomes restricted to IM cells, essential for subsequent urogenital development. Earlier markers like Odd1 (Osr1) emerge shortly after closure, with expression patterns broadening slightly before refining to the IM by the 6-somite stage, reflecting the spatiotemporal coordination of inductive signals. Modulation of signaling thresholds further refines IM specification by inhibiting alternative fates. High levels of Wnt signaling promote paraxial mesoderm formation and thus inhibit IM adoption by favoring somitic derivatives, whereas lower Wnt activity permits the intermediate positioning required for IM. Similarly, low BMP levels suppress lateral plate mesoderm fate by preventing excessive ventralization, allowing cells to adopt the intermediate identity when combined with appropriate Nodal inputs. Experimental studies in and have demonstrated the necessity of these signals for IM subtype specification. In , graded application of Nodal-related factors to animal cap explants induces IM markers like Pax2 at intermediate concentrations, with disruption of endogenous Nodal gradients via dominant-negative receptors abolishing IM formation while sparing paraxial fates. In , timed exposure to Nodal ligands specifies trunk mesoderm including IM precursors, and mutants lacking Vg1 exhibit severe reductions in IM-derived structures, underscoring the role of Vg1/Nodal heterodimers; BMP4 morphants similarly fail to properly segregate IM from lateral mesoderm during late gastrulation. These models highlight how precise spatiotemporal control of BMP4, Vg1, and Nodal ensures robust IM induction across species.

Urogenital Derivatives

Kidney Development

The intermediate mesoderm differentiates into the nephrogenic cord, which sequentially forms three kidney types in embryos: the pronephros, mesonephros, and metanephros, in a craniocaudal progression during early . This process begins in the fourth week and culminates in the functional adult by the end of the third , with each successive building on the remnants of the previous one while the earlier forms regress. The pronephros and mesonephros serve transient roles, whereas the metanephros persists as the definitive organ. The pronephros emerges around day 22 of as a transient structure in the region of the intermediate mesoderm, consisting of 7–10 pairs of rudimentary nephrotomes that form short tubules draining into the pronephric duct. This duct elongates caudally toward the but does not form functional nephrons in humans, serving no excretory role in mammals. By the end of week 4 (around day 28), the pronephros fully degenerates, leaving the pronephric duct (later renamed the ) as its primary legacy for subsequent . The mesonephros develops from weeks 4 to 8 in the thoracolumbar region of the intermediate mesoderm, caudal to the degenerating pronephros, and comprises approximately 30–40 pairs of S-shaped mesonephric tubules that connect to the . It functions temporarily as a primitive excretory organ, filtering small amounts of fluid into the between weeks 6 and 10, and also supports early hematopoiesis through the adjacent aorta-gonad-mesonephros region where hematopoietic stem cells emerge. Regression begins in week 8 and completes by week 16, with most structures degenerating in females while male remnants of the contribute to reproductive ducts. The metanephros, the permanent kidney, initiates in week 5 when the ureteric bud outgrowth from the invades the metanephric derived from the caudal intermediate mesoderm, triggering reciprocal inductive interactions that drive . The ureteric bud branches iteratively to form the collecting system (, renal pelvis, calyces, and collecting ducts), while condensed metanephric differentiates into nephrons, including glomeruli and tubules, with initial functional units appearing by week 11. Key milestones include the kidney's reniform shape by week 6, ascent from the pelvis to the region by week 9, and ongoing nephrogenesis with glomerular vascularization and tubular maturation until week 34–36, after which no new nephrons form postnatally. Transcription factors such as Pax2, expressed in the ureteric bud and ducts, and WT1, in the metanephric , are essential for these inductive processes. By week 36, the metanephros is structurally mature, capable of full filtration and endocrine functions.

Gonadal Ridge Formation

The gonadal ridge emerges during the fourth to fifth week of as a thickening of the coelomic overlying the intermediate mesoderm, located medial to the mesonephros and forming paired urogenital ridges along the posterior . This involves coelomic epithelial cells undergoing epithelial-mesenchymal transition to contribute mesenchymal components, establishing the primordium of the bipotential . By the end of the fifth week, the ridge is histologically identifiable as a longitudinal elevation with an outer epithelial layer and underlying derived from the intermediate mesoderm. Primordial germ cells (PGCs), originating in the during the third week, migrate toward the gonadal ridge via the dorsal mesentery and , reaching the ridge between weeks 5 and 6. This is guided by chemotactic signals such as KIT ligand and SDF-1/, with PGCs proliferating to approximately 1,000–2,000 cells upon arrival and integrating with the cells of the ridge to form the early gonadal . By week 6, the PGCs are fully incorporated, marking the completion of ridge colonization and the onset of germ cell-soma interactions essential for subsequent differentiation. The gonadal ridge remains bipotential until approximately week 7, exhibiting no morphological sex differences and retaining the capacity to develop into either testes or ovaries. In embryos, activation of the gene on the around days 41–44 (late week 6 to early week 7) initiates male sex determination by upregulating , which promotes differentiation of pre-Sertoli cells and organization of testicular cords. In the absence of SRY in embryos, ovarian development proceeds, characterized by proliferation of surface epithelium and germ cells forming nests that subsequently break down to enable follicle assembly. Histological changes culminate in distinct gonadal structures: in testes, Sertoli cells aggregate around PGCs to form seminiferous cords by week 7–8, which canalize into tubules by week 9, accompanied by the emergence of Leydig cells and a fibrous tunica albuginea; in ovaries, germ cells enter by week 10, with germ cell nests disintegrating around weeks 12–16 to form primordial follicles enclosing and pre-granulosa cells, progressing to primary follicles by the fourth month. These timelines reflect the rapid transition from bipotentiality to sexually dimorphic organs, with full histological maturation continuing into the second trimester.

Reproductive Ducts and Associated Structures

The Wolffian ducts, also known as mesonephric ducts, originate from the intermediate mesoderm and form through the caudal of the pronephric duct during early embryonic development. In embryos, these ducts become visible by approximately 25 to 29 days post-fertilization, extending from the region near the future buds to the . This involves mesenchymal cell rearrangement via convergent extension mechanisms rather than proliferation, establishing a continuous tube that serves as a precursor for parts of the . In males, the Wolffian ducts persist and differentiate under the influence of testosterone produced by Leydig cells in the differentiating testes, beginning around week 7 of . This hormonal stabilization prevents regression and promotes the development of key structures, including the , , and , with differentiated forms evident by 8.5 to 9 weeks. Additionally, mesonephric tubules associated with the Wolffian duct contribute to male reproductive structures, such as the that connect the to the . In females, the Wolffian ducts undergo active degeneration starting around week 10, driven by factors like COUP-TFII, leaving only vestigial remnants such as the ducts. The Müllerian ducts, or paramesonephric ducts, arise independently as paired invaginations of the coelomic epithelium along the gonadal ridges around week 6 of . In females, these ducts grow caudally, fuse at their medial edges to form the uterovaginal , and differentiate into the fallopian tubes, , , and upper by approximately week 10, in the absence of (AMH). In males, AMH secreted by Sertoli cells initiates regression starting at week 7 (around 50-55 days), progressing through a fibroblastic ring-mediated process that leads to near-complete disappearance by week 10. This sex-specific fate determination of both duct systems, dependent on gonadal hormone production from week 6 onward, establishes the internal reproductive tracts by the end of the first trimester, coinciding with the regression of transient mesonephric structures.

Adrenal Cortex Development

The adrenal cortex arises from the intermediate mesoderm, specifically from mesodermal cells in the coelomic epithelium of the urogenital ridge. During the sixth week of (approximately 28-30 days post-conception), these cells thicken to form the adrenogonadal (AGP), a shared precursor structure located in close proximity to the developing gonadal ridge. This undergoes an epithelial-to-mesenchymal transition, enabling the cells to delaminate and migrate dorsally to establish the initial adrenal anlage. By weeks 7-8 of , the differentiates into two primary s: a large inner fetal , which predominates and drives early growth, and a thin outer definitive . Between weeks 8-10, the definitive begins to organize into rudimentary subzones that foreshadow the adult architecture, including the outer glomerulosa-like region for precursors, the fasciculata-like middle layer for synthesis, and an emerging reticularis-like inner area. Concurrently, steroidogenic cell differentiation initiates in the definitive , marked by expression of enzymes such as and P450c21, supporting the onset of hormone production. The entire structure becomes fully encapsulated by mesenchymal cells by the end of the ninth week. Vascular integration accompanies this early development, with the adrenal primordium supplied by arteries branching from the by the eighth week, facilitating nutrient delivery and secretion. Functional maturation progresses rapidly, enabling and production by the twelfth week of , primarily in the fetal zone for dehydroepiandrosterone sulfate and in the definitive zone for precursors under adrenocorticotropic regulation. In humans, steroidogenesis initiation is critically dependent on (SF-1, also known as NR5A1), a expressed from the AGP stage onward that drives the expression of key steroidogenic genes and ensures endocrine competence.

Regulatory Pathways and Markers

Key Transcription Factors

The intermediate mesoderm (IM) relies on a core set of transcription factors to establish and maintain its identity, directing differentiation toward urogenital lineages such as the nephric duct and metanephric . Among these, Osr1, Pax2, Lhx1, and WT1 play pivotal roles in specifying and restricting IM domains, with their expression patterns and regulatory functions conserved across vertebrates. These factors act in a hierarchical manner, often upstream of mesenchymal-to-epithelial transitions essential for . Osr1 (odd-skipped related 1) serves as one of the earliest specific markers for IM formation, emerging shortly after gastrulation in mouse, chick, and zebrafish embryos, where it demarcates a multipotent population within the lateral plate mesoderm that progresses to IM fate. By the 6-somite stage in mouse embryos, Osr1 expression activates downstream targets including Pax2 and Pax8, committing cells to the nephric lineage and enabling pronephric duct formation; Osr1 mutants exhibit reduced IM extent and failed nephric induction due to apoptosis in prospective IM cells. This factor is essential for the temporal dynamics of IM specification, inhibiting premature lateral venous plexus development while promoting nephrogenic potential, as evidenced by overexpression studies in Xenopus that enlarge pronephric structures. Pax2, a paired-box , is activated in the nascent around the 8-9 stage in mice, marking the pronephric anlage and functioning redundantly with to specify the nephric lineage from intermediate mesoderm. It regulates ureteric bud outgrowth by directly activating glial cell line-derived neurotrophic factor (Gdnf) expression in the metanephric mesenchyme, ensuring proper branching morphogenesis and reciprocal induction with the bud; Pax2 also coordinates segmentation by maintaining progenitor identity and promoting mesenchymal-to-epithelial transitions in renal vesicles. Mutations in PAX2 disrupt these processes, leading to renal-coloboma syndrome with defects and , underscoring its non-redundant role in later kidney patterning. Lhx1 (LIM homeobox 1), a LIM-domain homeodomain factor, is expressed broadly in early lateral plate mesoderm but becomes restricted to the IM domain post-gastrulation, around embryonic day 7.5 in mice, where it patterns the nephric field and prevents expansion into paraxial mesoderm territories. Essential for renal progenitor specification, Lhx1 depletion in Xenopus abolishes expression of IM markers like pax2 and pax8, resulting in loss of the kidney field, while overexpression expands IM at the expense of somitic fates. It is equally critical for gonadal formation, as Lhx1-null mice fail to develop functional kidneys and gonads due to defective Müllerian duct regression and genital ridge maintenance. WT1 (Wilms tumor 1), a zinc-finger , initiates expression in the coelomic overlying the IM around embryonic day 9.5 in mice, becoming prominent in the metanephric by day 11 and in the gonadal by day 10.5, where it drives epithelial transitions in both renal vesicles and somatic gonadal cells. In the , WT1 is detected in condensing metanephric , S-shaped bodies, and maturing podocytes, promoting mesenchymal and glomerular ; in human embryos, similar patterns appear by week 5, with WT1+ cells in the nephrogenic zone and early glomeruli. For gonadal development, WT1 marks the in both sexes, persisting in Sertoli cells (males) and granulosa cells (females) to support thickening and sex-specific morphogenesis. WT1 isoforms, particularly the +KTS variant, facilitate these epithelial shifts by regulating and proliferation genes.

Signaling Pathways Involved

The canonical Wnt/β-catenin signaling pathway plays a pivotal role in the patterning and differentiation of intermediate mesoderm derivatives, particularly in driving nephron induction and ureteric bud branching during metanephros development. In the mouse model, stabilization of β-catenin in the metanephric mesenchyme is essential for the mesenchymal-to-epithelial transition that forms renal vesicles, as demonstrated by conditional knockout studies where loss of β-catenin leads to failure of nephron formation. This pathway also regulates ureteric bud branching morphogenesis by promoting the expression of branching factors in the ureteric epithelium, with ectopic Wnt activation resulting in supernumerary buds and renal hyperplasia. GDNF-Ret signaling constitutes a key reciprocal interaction between the metanephric and ureteric bud , essential for ureteric bud outgrowth and subsequent branching. Glial cell line-derived neurotrophic factor (GDNF), secreted by the , binds to the Ret on ureteric bud s, activating downstream pathways such as PI3K and MAPK to promote and . In Ret knockout mice, ureteric bud formation is absent, leading to , underscoring the pathway's necessity for initiating organogenesis from intermediate mesoderm. Anterior-posterior patterning of the nephric segments—from pronephros to metanephros—relies on gradients of (FGF) and (RA) that regionalize the intermediate mesoderm along the body axis. Posterior FGF signaling, particularly FGF8, promotes elongation and segmentation of the nephric duct, while RA gradients, generated by Cyp26 enzymes, restrict anterior pronephric fates and stabilize posterior metanephric identity through regulation. Disruption of RA synthesis in models abolishes metanephric specification, highlighting its role in establishing segmental competence within the intermediate mesoderm lineage. In gonadal contexts, hedgehog signaling, primarily through Desert hedgehog (Dhh), supports sex determination by specifying fetal Leydig cell fate in the testis, derived from the gonadal ridge of intermediate mesoderm. Dhh, expressed by Sertoli cells, activates Patched1 receptors on interstitial progenitors to drive androgen production necessary for male differentiation; Dhh knockout mice exhibit disrupted Leydig cell differentiation and subsequent male gonadal defects, though initial ridge formation occurs normally. For adrenal cortex development, Sonic hedgehog (Shh) signaling from subcapsular cells patterns the provisional cortex and maintains progenitor pools, with Shh-null mice showing disorganized adrenal zonation and reduced steroidogenic capacity. These hedgehog pathways thus integrate with other signals to refine intermediate mesoderm-derived endocrine structures.

Clinical and Pathological Aspects

Congenital Anomalies

Congenital anomalies arising from disruptions in intermediate mesoderm development primarily manifest as structural defects in the renal and urogenital systems, reflecting the mesoderm's role in forming the metanephric blastema, nephric ducts, gonadal ridges, and adrenocortical primordia. These malformations often result from failures in , induction, or fusion during embryogenesis, leading to impaired and potential clinical complications such as renal dysfunction or reproductive tract abnormalities. Renal agenesis, characterized by the complete absence of one or both kidneys, stems from the failure of the ureteric bud to invade the metanephric mesenchyme derived from intermediate mesoderm, preventing nephrogenesis. Unilateral renal agenesis occurs in approximately 1 in 1,000 births and is often asymptomatic but associated with compensatory hypertrophy of the contralateral kidney, while bilateral renal agenesis is rarer at 1 in 3,000 to 4,000 newborns and is typically lethal due to oligohydramnios and pulmonary hypoplasia. Mutations in genes like PAX2, which regulate intermediate mesoderm patterning, have been implicated in such cases. Horseshoe kidney represents a fusion anomaly where the kidneys unite at their lower poles across the midline, arising from abnormal migration of the metanephric mesenchyme during ascent from the , a process originating in the intermediate mesoderm. This condition affects about 1 in 400 to 500 live births, making it the most common renal defect, and is often detected incidentally but predisposes individuals to urinary tract infections, stones, and due to altered pelvicalyceal orientation. Müllerian anomalies, such as uterine didelphys or , result from defective or resorption of the paramesonephric (Müllerian) ducts, which invaginate from the coelomic overlying the intermediate mesoderm-derived urogenital ridge. Uterine didelphys, involving two separate uteri and often duplicated vaginas, accounts for roughly 5% of such anomalies and can lead to reproductive challenges like preterm labor or . Mayer-Rokitansky-Küster-Hauser syndrome, featuring vaginal with variable uterine involvement, similarly disrupts normal female genital tract formation. Congenital adrenal hypoplasia involves underdevelopment of the , which originates from the intermediate mesoderm of the urogenital ridge, leading to insufficient and production and resultant . This rare condition, with an estimated incidence of 1 in 12,500 births in some populations, presents in infancy with salt-wasting crises, , and if untreated.

Associated Tumors and Disorders

The intermediate mesoderm gives rise to structures susceptible to various neoplastic and genetic disorders, particularly those affecting the kidneys, gonads, and . Among these, (nephroblastoma) is the most common pediatric renal malignancy, originating from metanephric blastemal cells that recapitulate embryonic nephrogenesis. It exhibits a characteristic triphasic comprising blastemal, epithelial, and stromal components, reflecting disrupted differentiation of intermediate mesoderm-derived progenitors. The incidence is approximately 1 in 10,000 children, with most cases diagnosed before age 5. Genetic alterations, including WT1 mutations, occur in 10-20% of sporadic cases, leading to loss of tumor suppressor function and promoting uncontrolled proliferation. Dysregulation of the Wnt pathway, often via CTNNB1 mutations, further contributes to tumorigenesis in a subset of tumors. Persistent Müllerian duct syndrome (PMDS) is a rare disorder of linked to intermediate mesoderm derivatives, where 46,XY individuals retain Müllerian structures such as the and fallopian tubes due to defective regression. It results from biallelic mutations in the AMH gene (encoding ) or AMHR2 gene (encoding its receptor), impairing signaling that normally induces Müllerian duct during embryogenesis. Affected males typically present with or , and diagnosis is confirmed through imaging revealing persistent Müllerian remnants alongside normal male external genitalia. Complications include and increased risk of gonadal tumors if undescended testes are present. Denys-Drash syndrome (DDS) represents a WT1-related arising from germline mutations in the WT1 gene, which is essential for intermediate mesoderm-derived urogenital development. It features a classic triad of progressive nephropathy due to diffuse mesangial sclerosis, leading to early renal failure; with ambiguous genitalia or female phenotype; and a markedly elevated risk of , approaching 90% in affected individuals. The nephropathy typically manifests in infancy with and , progressing to end-stage renal disease by age 3 in most cases. Tumor predisposition stems from WT1's role in suppressing nephrogenic proliferation, with mutations disrupting DNA binding and . Adrenocortical carcinoma (ACC) is a rare endocrine malignancy originating from the adrenal cortex, which derives from intermediate mesoderm during fetal development. It often arises from the fetal zone of the adrenal cortex, exhibiting aggressive behavior with local invasion and metastasis in over 50% of cases at diagnosis. Germline TP53 mutations, particularly in Li-Fraumeni syndrome, are implicated in up to 70-80% of pediatric ACC, while somatic TP53 alterations occur in 20-35% of sporadic tumors, driving oncogenesis through impaired cell cycle control and apoptosis. These tumors produce excess hormones like cortisol or androgens, contributing to clinical features such as virilization or Cushing syndrome in children.