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PubMed2005

Activation of mitogen activated protein kinase pathways and melanogenesis by novel nitro-derivatives of 7-hydroxycomarin in human malignant melanoma cells.

6-Nitro-7-hydroxycoumarin (6-NO2-7-OHC) and 3,6,8-trinitro-7-hydroxycoumarin (3,6,8-NO2-7-OHC) have previously been shown to be potent and selective anti-proliferative agents in a human melanoma cell line. These agents functioned by decreasing DNA synthesis, through an inhibition of the S phase regulatory protein, cyclin A. However, the key molecular target(s) for these drugs remained undefined. Here, we attempted to elucidate the exact nature of the relationship between drug exposure and signal transduction, particularly their effects on the mitogen activated protein kinase (MAPK) cascades, and the consequent effect on cell growth, death and differentiation. Comparative studies were carried out using 7-hydroxycoumarin (7-OHC). Both nitro-derivatives were found to alter the phosphorylation status of ERK1/ERK2 and p38. However, 7-OHC exerted this effect only at higher concentrations and longer incubation times. Also, none of the three drugs had any effect on SAPK phosphorylation. Tyrosinase activity assays and morphological studies were used to show drug-induced effects on cellular differentiation. Unlike 7-OHC, both 6-NO2-7-OHC and 3,6,8-NO2-7-OHC caused a dramatic increase in tyrosinase activity in a manner similar to the cAMP elevating agent, forskolin. Also, the MEK inhibitor (PD98059) in combination with nitro-derivatives stimulated an even greater increase in tyrosinase activity when compared to either drug. In addition, the p38 inhibitor (SB203580) reduced the activity of both drugs. Morphological examination of treated cells showed nitro-derivatives caused changes consistent with altered cellular differentiation. Taken together, we have established that exposure of human malignant melanoma cells to these drugs leads to a modulation of p38 MAP kinase phosphorylation. This implies that these drugs may function by altering both melanogenesis and cellular differentiation. However, their effect on the levels of these proteins rather than their phosphorylation status remains to be determined. Therefore, additional studies are underway in order to identify the exact binding partners for these drugs.

Antineoplastic Agents↗
PubMed1995

Cellular stresses differentially activate c-Jun N-terminal protein kinases and extracellular signal-regulated protein kinases in cultured ventricular myocytes.

Anisomycin or osmotic stress induced by sorbitol activated c-Jun N-terminal protein kinases (JNKs) in ventricular myocytes cultured from neonatal rat hearts. After 15-30 min, JNK was activated by 10-20-fold. Activation by anisomycin was transient, but that by sorbitol was sustained for at least 4 h. In-gel JNK assays confirmed activation of two renaturable JNKs of 46 and 55 kDa (JNK-46 and JNK-55, respectively). An antibody against human JNK1 immunoprecipitated JNK-46 activity. Endothelin-1, an activator of extracellular signal-regulated protein kinases (ERKs), also transiently activated JNKs by 2-5-fold after 30 min. Phorbol 12-myristate 13-acetate did not activate the JNKs although it activated ERK1 and ERK2, which phosphorylated the c-Jun transactivation domain in vitro. ATP depletion and repletion achieved by incubation in cyanide+deoxyglucose and its subsequent removal from the medium activated the ERKs but failed to activate the JNKs. Sorbitol (but not anisomycin) also stimulated the ERKs. Sorbitol-stimulated JNK activity could be resolved into three peaks by fast protein liquid chromatography on a Mono Q column. The two major peaks contained JNK-46 or JNK-55. These results demonstrate that cellular stresses differentially activate the JNKs and ERKs and that there may be "cross-talk" between these MAPK pathways.

Amino Acid Sequence↗
PubMed1997

Molecular characterization of glioblastoma cell differentiation.

OBJECTIVE: Induction of cellular differentiation continues to be an attractive therapeutic strategy for malignant glioma. The purpose of this study was to develop a convenient in vitro model system for glioblastoma differentiation and to then characterize it using conventional techniques and flow cytometry. METHODS: A subline of U138 MG cells ("U138B") was treated with 0 to 4 mmol/L sodium butyrate (or serum deprivation) for up to 96 hours. Cells were initially studied for effects on proliferation, morphology, and glial fibrillary acidic protein (GFAP) staining. Northern blot and immunoblot analyses of c-myc expression were performed. Multiparameter flow cytometry was then used to analyze GFAP, c-myc protein, and total cellular protein fluorescence and to relate them to changes in cell cycle distribution. RESULTS: Butyrate treatment produced a dose-dependent inhibition of cellular proliferation and changes in morphology, GFAP staining, and c-myc expression consistent with a differentiation response. Detailed flow cytometric studies, including subpopulation analysis, showed that during 72 hours of treatment with 2 mmol/L butyrate, mean GFAP fluorescence increased to 420%, whereas c-myc protein decreased to 45 +/- 13% and total cellular protein increased to 181 +/- 17%. The effects of butyrate were distinct from those of serum deprivation and were not simply the result of cells shifting into Gzero/G1. CONCLUSION: The butyrate-induced responses of the U138B cell line provide a convenient model system for studying the molecular events accompanying the differentiation of glioblastoma cells. Multiparameter flow cytometry is a useful technique for characterizing such differentiation.

Biomarkers, Tumor↗
PubMedDate not supplied

Proliferation and substrate effects on endothelial cell thrombogenicity.

The effects of the cellular differentiation status and the adhesive-substrate on endothelial cell function in cell culture were measured with an enzyme based assay of surface thrombogenicity. A solid plastic, microporous polymeric, and fibronectin (FN) treated microporous polymeric were used as substrates for growth of endothelial cells. The microporous and FN treated synthetic substrates have been shown to aid in the induction of cellular differentiation mechanisms. Cells were studied under proliferative and nonproliferative growth conditions. The thrombogenicity of the surface created by the endothelial cell monolayers under various experimental conditions was determined using an enzyme based assay of fibrin deposition. Actively proliferating cells on the solid plastic substrate produced the most thrombogenic surface, while confluent endothelial cell monolayers grown on FN treated microporous substrate were the least thrombogenic surfaces. These data suggest that endothelial cell surface thrombogenicity is under substrate control, and also related to the cellular differentiation status. These findings are being used to design a novel approach to the small diameter synthetic vascular graft problem.

Animals↗
PubMed1999

Inhibiting gap junctional intercellular communication alters expression of differentiation markers in osteoblastic cells.

Gap junctional intercellular communication (GJIC) may contribute to cellular differentiation. To examine this possibility in bone cells we examined markers of cellular differentiation, including alkaline phosphatase, osteocalcin, and osteopontin, in ROS17/2.8 cells (ROS), a rat osteoblastic cell line expressing phenotypic characteristics of fully differentiated osteoblasts. We utilized ROS rendered communication deficient either by stable transfection with antisense cDNA to connexin 43 (Cx43), the predominant gap junction protein in bone (RCx16 cells), or by overexpression of Cx45, a gap junction protein not normally expressed in ROS (ROS/Cx45 cells). Both RCx16 and ROS/Cx45 cells displayed reduced dye coupling and Cx43 protein expression relative to ROS, control transfectants, and ROS/Cx45tr, ROS cells expressing carboxylterminal truncated Cx45. Steady-state mRNA levels for osteocalcin as well as alkaline phosphatase activity, two markers of osteoblastic differentiation, were also reduced in poorly coupled RCx16 and ROS/Cx45 cells. On the other hand, steady-state mRNA levels for osteopontin increased slightly in RCx16 and ROS/Cx45 cells. These results suggest that GJIC at least partly contributes to the regulation of expression of markers of osteoblastic differentiation.

Alkaline Phosphatase↗
PubMed1992

Domain-specific and cell type-specific localization of two types of cell wall matrix polysaccharides in the clover root tip.

Using immunocytochemical techniques and antibodies that specifically recognize xyloglucan (anti-XG), polygalacturonic acid/rhamnogalacturonan I (anti-PGA/RG-I), and methylesterified pectins (JIM 7), we have shown that these polysaccharides are differentially synthesized and localized during cell development and differentiation in the clover root tip. In cortical cells XG epitopes are present at a threefold greater density in the newly formed cross walls than in the older longitudinal walls, and PGA/RG-I epitopes are detected solely in the expanded middle lamella of cortical cell corners, even after pretreatment of sections with pectinmethylesterase to uncover masked epitopes. These results suggest that in cortical cells XG and PGA/RG-I are differentially localized not only to particular wall domains, but also to particular cell walls. In contrast to their nonoverlapping distribution in cortical cells, XG epitopes and PGA/RG-I epitopes largely colocalize in the epidermal cell walls. The results also demonstrate that the middle lamella of the longitudinal walls shared by epidermal cells and by epidermal and cortical cells constitutes a barrier to the diffusion of cell wall and mucilage molecules. Synthesis of XG and PGA/RG-I epitope-containing polysaccharides also varies during cellular differentiation in the root cap. The differentiation of gravitropic columella cells into mucilage-secreting peripheral cells is marked by a dramatic increase in the synthesis and secretion of molecules containing XG and PGA/RG-I epitopes. In contrast, JIM 7 epitopes are present at abundant levels in columella cell walls, but are not detectable in peripheral cell walls or in secreted mucilage. There were also changes in the cisternal labeling of the Golgi stacks during cellular differentiation in the root tip. Whereas PGA/RG-I epitopes are detected primarily in cis- and medial Golgi cisternae in cortical cells (Moore, P. J., K. M. M. Swords, M. A. Lynch, and L. A. Staehelin. 1991. J. Cell Biol. 112:589-602), they are localized predominantly in the trans-Golgi cisternae and the trans-Golgi network in epidermal and peripheral root cap cells. These observations suggest that during cellular differentiation the plant Golgi apparatus can be both structurally and functionally reorganized.

Antibodies, Monoclonal↗
PubMed2001

[Incidental diagnosis of renal carcinoma. Does it imply a better prognosis?].

OBJECTIVE: We present 267 patients undergoing surgery for renal carcinoma, comparing the incidental tumour and symptomatic tumour with different parameters and evaluating the prognostic significance of the incidental diagnosis. MATERIAL AND METHODS: Of the 267 patients, 110 (41.2%) were diagnosed incidentally. The different variables analysed were: age, sex, tumour size, if unilateral or bilateral, histological type, stage, degree of cellular differentiation and survival. The mean follow-up period was of 43.32 mos in the symptomatic patients and 41.85 mos in the patients diagnosed incidentally. The data obtained was analysed with the SPSS statistic pack. RESULTS: No significant difference was detected between both groups in regards to age, sex, if unilateral or bilateral and histological type. Comparing tumour size, a statistic difference was observed with slices at 6 cm. When analysing the stage and degree of cellular differentiation, a significant difference is found with tumours diagnosed incidentally presenting better differentiation and a lower stage at the moment of diagnosis. Survival after 5 yrs was of 65.7% for symptomatic patients in comparison to 81.7% for the incidental group, which implies high statistical signification (log rank = 0.0018). CONCLUSIONS: In our series no significant differences were detected between incidental and symptomatic tumours when comparing age, sex, anatomic side and histological type. Significant differences were indeed detected in relation to size, degree of cellular differentiation, tumour stage and survival.

Female↗
PubMed2001

Expression characteristics of the transfer-related kilB gene product of Streptomyces plasmid pIJ101: implications for the plasmid spread function.

Intermycelial transfer of Streptomyces plasmid pIJ101 occurs prior to cellular differentiation and is mediated by plasmid functions that are also required for production of zones of growth-inhibited recipient cells (i.e., pocks) that develop around individual donors during mating on agar medium. Several other pIJ101 functions, including that of the kilB gene, whose unregulated expression on pIJ101 is lethal, are required for normal pock size and so have been postulated to mediate intramycelial spread of the plasmid throughout recipient cells. Using antibodies raised against a KilB fusion protein expressed in Escherichia coli, native KilB protein was detected throughout development of pIJ101-containing Streptomyces lividans cells, with the concentration of KilB increasing dramatically and reaching a maximum during the final stages (i.e., sporulation and secondary metabolism) of cellular differentiation. Insertion of the kilB gene of pIJ101 into the S. lividans chromosome in cells lacking the pIJ101 KorB protein, which normally represses kilB gene transcription, resulted in elevated but still temporally increasing amounts of KilB. The increased expression or accumulation of the KilB spread protein throughout cellular differentiation of S. lividans, which leads to maximum KilB concentrations during developmental stages that occur far later than when intermycelial transfer of pIJ101 is mediated, supports the existence of a subsequent intramycelial component to the pIJ101 spread function. The results also suggest that intramycelial spread of pIJ101 molecules within the recipient extends beyond intercompartmental movements within the substrate mycelia and includes undetermined steps within the spore-yielding aerial hyphae as well.

Bacterial Proteins↗
PubMed1988

Differential requirements for cellular enhancers in stem and differentiated cells.

Multiple cis-acting regulatory elements consisting of three cellular enhancers and a proximal promoter element have been identified in the region upstream of the mouse alpha-fetoprotein (AFP) gene. We examined the role of these sequences during differentiation by the introduction of modified AFP genes into cells at different stages of commitment to its expression. Modified AFP genes introduced stably into F9 embryonal carcinoma stem cells by DNA transfection were silent until activated by treatment with retinoic acid to form visceral endoderm. Their activation required the presence of both the enhancer and proximal promoter domains. The introduced genes activated simultaneously with the endogenous AFP genes, but reached maximal levels of expression more rapidly, suggesting a greater initial accessibility to transcription factors. In contrast, when modified AFP genes were stably introduced into HepG2 cells, a human hepatoma cell line that constitutively expresses the AFP gene, the proximal promoter sequences were sufficient to direct a low level of expression. The absolute requirement for the AFP enhancers in F9 cells but not in HepG2 cells supports a model by which there is an obligate requirement for enhancers during differentiation in addition to their role in enhancing gene expression after differentiation.

Animals↗
PubMed1998

Clinical utility of flexible bronchoscopy and bronchoalveolar lavage in young children with recurrent wheezing.

OBJECTIVE: The objective of this study was to determine in young children with recurrent wheezing poorly responsive to bronchodilator therapy whether flexible bronchoscopy (FB) and bronchoalveolar lavage (BAL) provide clinically useful information, whether age-specific differences are present in bronchoscopic and BAL fluid (BALF) findings, and whether differential cellular analysis of BALF is useful in suggesting an infectious or inflammatory process. DESIGN: This was a retrospective case series with descriptive and analytical components. The study population included children referred to a large tertiary care children's hospital subspecialty service for further evaluation of recurrent wheezing. Clinical and demographic data and findings of FB and BALF studies were collected from chart review. For purposes of data analysis patients were divided into 0- to 6-, 7- to 12-, and 13- to 18-month age groups. RESULTS: Thirty otherwise healthy children, 0 to 18 months of age with recurrent wheezing, who had undergone FB were identified; and 28 were found to have positive diagnostic findings. Airway abnormalities were found in 17 (57%) and tended to be more common in the 0- to 6-month age group. In the 27 who also had BAL performed, 3 (11%) had a positive bacterial culture, 9 (33%) a positive viral culture, and 5 (19%) an elevated lipid-laden macrophage index suggesting aspiration. Differential cellular analysis was abnormal in 11 (41%), a finding that was significantly associated with a positive bacterial culture, a positive viral culture, or an elevated lipid-laden macrophage index. CONCLUSIONS: In this population of young children with recurrent wheezing poorly responsive to bronchodilator therapy, FB and BAL yielded useful diagnostic findings in most children studied. In addition, in the presence of an infectious or inflammatory process, differential cellular analysis of BALF revealed an increased percentage of neutrophils.

Bronchoalveolar Lavage↗
PubMed2005

Bis induces growth inhibition and differentiation of HL-60 cells via up-regulation of p27.

Bis (Bag-3, CAIR), a Bcl-2-interacting protein, promotes the anti-apoptotic activity of Bcl-2 and increased levels of Bis have been observed in several disease models. The involvement of Bcl-2 and some Bcl-2-binding proteins in differentiation has recently been reported. However, the relevance of Bis to cellular differentiation remains unknown. The findings herein show that Bis expression is up-regulated during the differentiation of HL-60 cells. To investigate the effect of Bis expression on differentiation, we established Bis-overexpressing HL-60 cells (HL-60-bis). HL-60-bis cells have a low nuclear: cytoplasmic ratio and indented nucleus in Wright- Giemsa staining, and an increased expression of CD11b in immunofluorescence study, indicating the promotion of differentiation. The overexpression of Bis also resulted in a retarded cell growth rate, accompanied by the accumulation of HL-60 cells at the G0/G1 phase of the cell cycle, which was sustained during the differentiation process. Western blot analysis revealed that the expression of p27, a representative inducer of cell cycle arrest at the G1 phase, was increased 2.5-fold in HL-60-bis cells compared to HL-60-neo cells. These results suggest that the Bis induced growth inhibition of HL-60 cells promotes G0/G1 phase arrest via up-regulation of p27, which seems to be a prerequisite for differentiation. Further studies will be required to define the exact roles of Bis on cellular differentiation more precisely.

Adaptor Proteins, Signal Transducing↗
PubMed1989

Cell proliferation and differentiation in squamous cancer.

Cellular differentiation is generally regarded as an important histological predictor of tumour behaviour. Verrucous carcinoma is a very well-differentiated tumour characterised by slow enlargement and an unsatisfactory response to radiotherapy. Tumour cell kinetic studies using the intravenous administration of bromodeoxyuridine (BrdUrd) before tumour sampling have shown these tumours to have high labelling indices and short duration of DNA synthesis. These values result in short potential cell doubling times of these tumours although they then have a well-differentiated appearance histologically. Study of 20 other squamous cell carcinomas has shown no relationship between grade and cell proliferation.

Bromodeoxyuridine↗
PubMed2003

The fate and function of glycosphingolipid glucosylceramide.

In higher eukaryotes, glucosylceramide is the simplest member and precursor of a fascinating class of membrane lipids, the glycosphingolipids. These lipids display an astounding variation in their carbohydrate head groups, suggesting that glycosphingolipids serve specialized functions in recognition processes. It is now realized that they are organized in signalling domains on the cell surface. They are of vital importance as, in their absence, embryonal development is inhibited at an early stage. Remarkably, individual cells can live without glycolipids, perhaps because their survival does not depend on glycosphingolipid-mediated signalling mechanisms. Still, these cells suffer from defects in intracellular membrane transport. Various membrane proteins do not reach their intracellular destination, and, indeed, some intracellular organelles do not properly differentiate to their mature stage. The fact that glycosphingolipids are required for cellular differentiation suggests that there are human diseases resulting from defects in glycosphingolipid synthesis. In addition, the same cellular differentiation processes may be affected by defects in the degradation of glycosphingolipids. At the cellular level, the pathology of glycosphingolipid storage diseases is not completely understood. Cell biological studies on the intracellular fate and function of glycosphingolipids may open new ways to understand and defeat not only lipid storage diseases, but perhaps other diseases that have not been connected to glycosphingolipids so far.

Animals↗
PubMed2006

Cellular proliferation, differentiation and apoptosis in polyether-polyurethane sponge implant model in mice.

The integration of implanted material to host organism requires spatial and temporal organization of several cellular processes, such as proliferation, differentiation and apoptosis. Despite the clinical relevance of these processes, there is little information regarding the sequence of such events in synthetic matrices. Here, we present a combination of techniques used to characterize the fibrovascular response in subcutaneous polyether-polyurethane sponge implants in mice at days 4, 7, 10 and 14 postimplantation. The AgNOR technique was modified and used as a surrogate marker for proliferating and activated cells invading the implant. The number of AgNOR-stained cells increased progressively from day 4 (606+/-76) to day 14 (2146+/-71) postimplantation. The number of TUNEL-positive (apoptotic index) cells also increased progressively from day 4 (459+/-40) to day 14 (1157+/-119) postimplantation. However, the ratio of TUNEL-labeled/proliferating cells had its highest peak in the early phase of the process remaining stable until day 14. Using Picrosirius staining it was shown that thin collagen increased from day 4, peaking at day 10 and falling markedly at day 14, whereas dense collagen increased progressively during the whole period. These experiments hold potential to investigate not only distinct phases of tissue repair induced by synthetic matrices but also to study underlying mechanisms involved.

Animals↗
PubMed1990

[Cell proliferation in human cerebral tumors. In vivo study of 45 cases by incorporation of 5-iododesoxyuridine].

A method to study the proliferation of human brain tumors, is presented. Non radioactive 5-Iododeoxyuridine (2.4 gr) infused over a 24 hours period is detected in situ on histologic section by an immunological technique (peroxidase-anti-peroxidase) using a specific anti-Iododeoxyuridine antibody. This exploration utilised in 45 patients is easy, reliable and harmless. All cells which enter in S phase of cellular cycle during the infusion are labelled. So the cellular kinetics of all the brain tumor cells (malignant cells, inflammatory stroma reaction cells, reactive astrocytes, endothelial and muscular cells of the vessels) are detected on the same histological section, as well as all the others proliferative cells of the body (leukocytes, primitive tumor of the metastatic brain localisation...) if multiples biopsies are done. 8 of 9 gliomas of low histological malignancy (grade I and II) have a slow cellular kinetic. The 23 astrocytomas of different histological malignancy (grade III and IV) have variable proliferative speed (7 very fast, 8 fast and 8 slow). Only the large cells of the pinealoma are very proliferative, the lymphoid stroma is quiescent. The 5 metastasis have a slow to very fast kinetic without correlation with the cellular differentiation except in one case (important differentiation and slow cellular proliferation). The 5 lymphoma cells kinetics are well correlated with the histologic differentiation (3 large cells poor differentiated lymphomas and very fast kinetic, 2 better differentiated and slower proliferation). The 2 meningiomas proliferate slowly. The biochemical and histopathological grounds of the presented method and the limits of quantification are discussed. This method is compared with this using Bromodeoxyuridine. The correlation between proliferation and histologic malignancy is analysed. The use of cytokinetic results for therapeutic and prognosis need further statistical anatomoclinical studies.

Adult↗
PubMed1991

Expression of c-jun during macrophage differentiation of HL-60 cells.

Cellular transcription factors are important in the regulation of cellular genes. Recent studies have indicated that a class of cellular genes known as early response genes are important in the control of cellular growth properties. Two of these genes, c-jun and c-fos, play an important role in the control of cellular differentiation. Because the acute myelogenous leukemia cell line, HL-60, is capable of differentiating to either macrophages or granulocytes, it provides a good model to understand differential gene expression. To determine if the modulation of c-jun was important in the differentiation of HL-60 cells to either macrophages or granulocytes, expression of c-jun mRNA was determined by Northern analysis at various times following treatment with a variety of differentiating agents, including 12-tetradeconyl-phorbol 13-acetate (TPA), retinoic acid (RA), dimethyl sulfoxide (DMSO), or 1,25 dihydroxyvitamin D3 [1,25 (OH)2 D3]. Both TPA and 1,25(OH)2D3, which induce HL-60 cells to differentiate to macrophages, resulted in marked increases in c-jun mRNA; while RA and DMSO, which induce HL-60 cells to differentiate to granulocytes, did not greatly alter c-jun mRNA expression. HL-60 cell lines resistant to macrophage differentiation after exposure to either 1,25(OH)2D3 or TPA did not result in increases in c-jun mRNA. These results suggest that elevation of c-jun mRNA in HL-60 cells correlated temporally with differentiation to macrophages. Thus, c-jun may be a critical cellular transcription factor involved in macrophage differentiation.

Calcitriol↗
PubMed1996

Dopamine receptors mediate differential morphological effects on cerebral cortical neurons in vitro.

A morphogenic role of neurotransmitters during cellular differentiation in vitro has been demonstrated in recent years. Using in situ hybridization, we confirm the presence of the D1 receptor at E16 and show additionally that the transcript is relatively widespread and present in both proliferative and differentiating areas of the cerebral wall. Because DA receptor expression precedes the arrival of presynaptic terminals during forebrain development, we examined the role of DA in cerebral cortical neuron differentiation in vitro, using immunohistochemical markers of dendrites, microtubule-associated-membrane protein 2 (MAP2) and axons, neurofilament protein (NF-H). Neurite length, cell size, and cell viability in response to D1 and D2 receptor agonists SKF38393 and quinpirole, respectively, and to DA were analyzed in neurons obtained from embryonic (E) day 16 rats. We have shown that 1) paradoxically, DA at different concentrations can either stimulate or inhibit neurite outgrowth; 2) there is a bimodal pattern of DA-induced axonal outgrowth, i.e., at low and high doses; 3) D2 receptor activation induces neurite outgrowth while D1 receptor activation is inhibitory; 4) D2-mediated neurite elongation is preferentially axonal while D1 receptor activation reduces both axonal and dendritic outgrowth; 5) low doses of DA promote the expression of cytoskeletal components of axonal maturation; and 6) D1 receptor activation decreases neuronal size. We suggest that DA may influence cellular differentiation and circuitry formation early in development of the cerebral cortex through receptor-mediated effects on process outgrowth, which could lead to effects on circuit formation.

Animals↗