Sexual dimorphisms in adult human neural, mesoderm-derived, and neural crest-derived stem cells.
NF-κB
mesoderm-derived stem cells
neural crest-derived stem cells
neural stem cells
neurocristopathies
neuroprotection
sex-specific differences
stem cells
Journal
FEBS letters
ISSN: 1873-3468
Titre abrégé: FEBS Lett
Pays: England
ID NLM: 0155157
Informations de publication
Date de publication:
12 2019
12 2019
Historique:
received:
28
06
2019
revised:
03
09
2019
accepted:
05
09
2019
pubmed:
19
9
2019
medline:
20
6
2020
entrez:
19
9
2019
Statut:
ppublish
Résumé
Sexual dimorphisms contribute, at least in part, to the severity and occurrence of a broad range of neurodegenerative, cardiovascular, and bone disorders. In addition to hormonal factors, increasing evidence suggests that stem cell-intrinsic mechanisms account for sex-specific differences in human physiology and pathology. Here, we discuss sex-related intrinsic mechanisms in adult stem cell populations, namely mesoderm-derived stem cells, neural stem cells (NSCs), and neural crest-derived stem cells (NCSCs), and their implications for stem cell differentiation and regeneration. We particularly focus on sex-specific differences in stem cell-mediated bone regeneration, in neuronal development, and in NSC-mediated neuroprotection. Moreover, we review our own recently published observations regarding the sex-dependent role of NF-κB-p65 in neuroprotection of human NCSC-derived neurons and sex differences in NCSC-related disorders, so-called neurocristopathies. These observations are in accordance with the increasing evidence pointing toward sex-specific differences in neurocristopathies and degenerative diseases like Parkinson's disease or osteoporosis. All findings discussed here indicate that sex-specific variability in stem cell biology may become a crucial parameter for the design of future treatment strategies.
Identifiants
pubmed: 31529465
doi: 10.1002/1873-3468.13606
doi:
Substances chimiques
NF-kappa B
0
eIF-2 Kinase
EC 2.7.11.1
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
3338-3352Informations de copyright
© 2019 The Authors. FEBS Letters published by John Wiley & Sons Ltd on behalf of Federation of European Biochemical Societies.
Références
Aristotle (350 BC). Historia Animalium: Books VII-X. Harvard University Press, Cambridge, MA.
Avery B, Jorgensen CB, Madison V and Greve T (1992) Morphological development and sex of bovine in vitro-fertilized embryos. Mol Reprod Dev 32, 265-270.
Kochhar HS, Kochhar KP, Basrur PK and King WA (2003) Influence of the duration of gamete interaction on cleavage, growth rate and sex distribution of in vitro produced bovine embryos. Anim Reprod Sci 77, 33-49.
Xu KP, Yadav BR, King WA and Betteridge KJ (1992) Sex-related differences in developmental rates of bovine embryos produced and cultured in vitro. Mol Reprod Dev 31, 249-252.
Gutierrez-Adan A, Oter M, Martinez-Madrid B, Pintado B and De La Fuente J (2000) Differential expression of two genes located on the X chromosome between male and female in vitro-produced bovine embryos at the blastocyst stage. Mol Reprod Dev 55, 146-151.
Barnes LL, Wilson RS, Bienias JL, Schneider JA, Evans DA and Bennett DA (2005) Sex differences in the clinical manifestations of Alzheimer disease pathology. Arch Gen Psychiatry 62, 685-691.
Schultz C, Braak H and Braak E (1996) A sex difference in neurodegeneration of the human hypothalamus. Neurosci Lett 212, 103-106.
Kher A, Wang M, Tsai BM, Pitcher JM, Greenbaum ES, Nagy RD, Patel KM, Wairiuko GM, Markel TA and Meldrum DR (2005) Sex differences in the myocardial inflammatory response to acute injury. Shock 23, 1-10.
Vaccarino V, Krumholz HM, Berkman LF and Horwitz RI (1995) Sex differences in mortality after myocardial infarction. Is there evidence for an increased risk for women? Circulation 91, 1861-1871.
Eugene D, Djemli A and Van Vliet G (2005) Sexual dimorphism of thyroid function in newborns with congenital hypothyroidism. J Clin Endocrinol Metab 90, 2696-2700.
Choudhry MA, Bland KI and Chaudry IH (2006) Gender and susceptibility to sepsis following trauma. Endocr Metab Immune Disord Drug Targets 6, 127-135.
van Wessum R, Harvey CE and Hennet P (1992) Feline dental resorptive lesions. Prevalence patterns. Vet Clin North Am Small Anim Pract 22, 1405-1416.
Crisostomo PR, Markel TA, Wang M, Lahm T, Lillemoe KD and Meldrum DR (2007) In the adult mesenchymal stem cell population, source gender is a biologically relevant aspect of protective power. Surgery 142, 215-221.
Deasy BM, Lu A, Tebbets JC, Feduska JM, Schugar RC, Pollett JB, Sun B, Urish KL, Gharaibeh BM, Cao B et al. (2007) A role for cell sex in stem cell-mediated skeletal muscle regeneration: female cells have higher muscle regeneration efficiency. J Cell Biol 177, 73-86.
Nakada D, Oguro H, Levi BP, Ryan N, Kitano A, Saitoh Y, Takeichi M, Wendt GR and Morrison SJ (2014) Oestrogen increases haematopoietic stem-cell self-renewal in females and during pregnancy. Nature 505, 555-558.
Ray R, Novotny NM, Crisostomo PR, Lahm T, Abarbanell A and Meldrum DR (2008) Sex steroids and stem cell function. Mol Med 14, 493-501.
Zhou S, Zilberman Y, Wassermann K, Bain SD, Sadovsky Y and Gazit D (2001) Estrogen modulates estrogen receptor alpha and beta expression, osteogenic activity, and apoptosis in mesenchymal stem cells (MSCs) of osteoporotic mice. J Cell Biochem Suppl Suppl 36, 144-155.
Marin-Husstege M, Muggironi M, Raban D, Skoff RP and Casaccia-Bonnefil P (2004) Oligodendrocyte progenitor proliferation and maturation is differentially regulated by male and female sex steroid hormones. Dev Neurosci 26, 245-254.
Carreras E and Kovats S (2014) Girl power: estrogen promotes HSC self-renewal. Cell Stem Cell 14, 137-138.
Leeman DS and Brunet A (2014) Stem cells: sex specificity in the blood. Nature 505, 488-490.
Kyo S, Takakura M, Kanaya T, Zhuo W, Fujimoto K, Nishio Y, Orimo A and Inoue M (1999) Estrogen activates telomerase. Can Res 59, 5917-5921.
Dulken B and Brunet A (2015) Stem Cell Aging and Sex: are We Missing Something? Cell Stem Cell 16, 588-590.
Tamaki S, Ichinohe T, Matsuo K, Hamajima N, Hirabayashi N, Dohy H and Japan Society of Hematopoietic Cell Transplantation (2001). Superior survival of blood and marrow stem cell recipients given maternal grafts over recipients given paternal grafts. Bone Marrow Transplant 28, 375-380.
Blankenhorn EP, Troutman S, Clark LD, Zhang XM, Chen P and Heber-Katz E (2003) Sexually dimorphic genes regulate healing and regeneration in MRL mice. Mamm Genome 14, 250-260.
Govindarajan P, Bocker W, El Khassawna T, Kampschulte M, Schlewitz G, Huerter B, Sommer U, Durselen L, Ignatius A, Bauer N et al. (2014) Bone matrix, cellularity, and structural changes in a rat model with high-turnover osteoporosis induced by combined ovariectomy and a multiple-deficient diet. Am J Pathol 184, 765-777.
Newton BI, Cooper RC, Gilbert JA, Johnson RB and Zardiackas LD (2004) The ovariectomized sheep as a model for human bone loss. J Comp Pathol 130, 323-326.
Wang L, Zhao Y, Liu Y, Akiyama K, Chen C, Qu C, Jin Y and Shi S (2013a) IFN-gamma and TNF-alpha synergistically induce mesenchymal stem cell impairment and tumorigenesis via NFkappaB signaling. Stem Cells 31, 1383-1395.
Kitajima Y, Doi H, Ono Y, Urata Y, Goto S, Kitajima M, Miura K, Li TS and Masuzaki H (2015) Estrogen deficiency heterogeneously affects tissue specific stem cells in mice. Sci Rep 5, 12861.
Bramble MS, Roach L, Lipson A, Vashist N, Eskin A, Ngun T, Gosschalk JE, Klein S, Barseghyan H, Arboleda VA et al. (2016) Sex-Specific Effects of Testosterone on the Sexually Dimorphic Transcriptome and Epigenome of Embryonic Neural Stem/Progenitor Cells. Sci Rep 6, 36916.
Bramble MS, Vashist N and Vilain E (2019) Sex steroid hormone modulation of neural stem cells: a critical review. Biol Sex Differ 10, 28.
Parker MJ, Raghavan R and Gurusamy K (2007) Incidence of fracture-healing complications after femoral neck fractures. Clin Orthop Relat Res 458, 175-179.
Strube P, Mehta M, Baerenwaldt A, Trippens J, Wilson CJ, Ode A, Perka C, Duda GN and Kasper G (2009) Sex-specific compromised bone healing in female rats might be associated with a decrease in mesenchymal stem cell quantity. Bone 45, 1065-1072.
Pien DM, Olmedo DG and Guglielmotti MB (2001) Influence of age and gender on peri-implant osteogenesis. Age and gender on peri-implant osteogenesis. Acta Odontol Latinoam 14, 9-13.
Cawthon PM (2011) Gender differences in osteoporosis and fractures. Clin Orthop Relat Res 469, 1900-1905.
Ejiri S, Tanaka M, Watanabe N, Anwar RB, Yamashita E, Yamada K and Ikegame M (2008) Estrogen deficiency and its effect on the jaw bones. J Bone Miner Metab 26, 409-415.
Wang X, Wang Y, Gou W, Lu Q, Peng J and Lu S (2013b) Role of mesenchymal stem cells in bone regeneration and fracture repair: a review. Int Orthop 37, 2491-2498.
Aksu AE, Rubin JP, Dudas JR and Marra KG (2008) Role of gender and anatomical region on induction of osteogenic differentiation of human adipose-derived stem cells. Ann Plast Surg 60, 306-322.
Corsi KA, Pollett JB, Phillippi JA, Usas A, Li G and Huard J (2007) Osteogenic potential of postnatal skeletal muscle-derived stem cells is influenced by donor sex. J Bone Miner Res 22, 1592-1602.
Muschler GF, Nitto H, Boehm CA and Easley KA (2001) Age- and gender-related changes in the cellularity of human bone marrow and the prevalence of osteoblastic progenitors. J Orthop Res 19, 117-125.
Crisostomo PR, Wang M, Herring CM, Morrell ED, Seshadri P, Meldrum KK and Meldrum DR (2006) Sex dimorphisms in activated mesenchymal stem cell function. Shock 26, 571-574.
Ruiz-Perera LM, Schneider L, Windmoller BA, Muller J, Greiner JFW, Kaltschmidt C and Kaltschmidt B (2018) NF-kappaB p65 directs sex-specific neuroprotection in human neurons. Sci Rep 8, 16012.
Kiss DL, Xu W, Gopalan S, Buzanowska K, Wilczynska KM, Rydel RE and Kordula T (2005) Duration of alpha 1-antichymotrypsin gene activation by interleukin-1 is determined by efficiency of inhibitor of nuclear factor kappa B alpha resynthesis in primary human astrocytes. J Neurochem 92, 730-738.
Ishida M, Kawao N, Okada K, Tatsumi K, Sakai K, Nishio K and Kaji H (2018) Serpina3n, dominantly expressed in female osteoblasts, suppresses the phenotypes of differentiated osteoblasts in mice. Endocrinology 159, 3775-3790.
Lu X, Gilbert L, He X, Rubin J and Nanes MS (2006) Transcriptional regulation of the osterix (Osx, Sp7) promoter by tumor necrosis factor identifies disparate effects of mitogen-activated protein kinase and NF kappa B pathways. J Biol Chem 281, 6297-6306.
Samant RS, Clark DW, Fillmore RA, Cicek M, Metge BJ, Chandramouli KH, Chambers AF, Casey G, Welch DR and Shevde LA (2007) Breast cancer metastasis suppressor 1 (BRMS1) inhibits osteopontin transcription by abrogating NF-kappaB activation. Mol Cancer 6, 6.
McCarthy MM and Arnold AP (2011) Reframing sexual differentiation of the brain. Nat Neurosci 14, 677-683.
Hillerer KM, Neumann ID, Couillard-Despres S, Aigner L and Slattery DA (2013) Sex-dependent regulation of hippocampal neurogenesis under basal and chronic stress conditions in rats. Hippocampus 23, 476-487.
Madeira MD and Paula-Barbosa MM (1993) Reorganization of mossy fiber synapses in male and female hypothyroid rats: a stereological study. J Comp Neurol 337, 334-352.
Tanapat P, Hastings NB, Reeves AJ and Gould E (1999) Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J Neurosci 19, 5792-5801.
Le Douarin NM and Smith J (1988) Development of the peripheral nervous system from the neural crest. Annu Rev Cell Biol 4, 375-404.
McKey J, Bunce C, Batchvarov IS, Ornitz DM and Capel B (2019) Neural crest-derived neurons invade the ovary but not the testis during mouse gonad development. Proc Natl Acad Sci USA 116, 5570-5575.
Du L, Bayir H, Lai Y, Zhang X, Kochanek PM, Watkins SC, Graham SH and Clark RS (2004) Innate gender-based proclivity in response to cytotoxicity and programmed cell death pathway. J Biol Chem 279, 38563-38570.
Miller IN and Cronin-Golomb A (2010) Gender differences in Parkinson's disease: clinical characteristics and cognition. Mov Disord 25, 2695-2703.
Spychala MS, Honarpisheh P and McCullough LD (2017) Sex differences in neuroinflammation and neuroprotection in ischemic stroke. J Neurosci Res 95, 462-471.
Circu ML and Aw TY (2010) Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic Biol Med 48, 749-762.
Schmeisser MJ, Baumann B, Johannsen S, Vindedal GF, Jensen V, Hvalby OC, Sprengel R, Seither J, Maqbool A, Magnutzki A et al. (2012) IkappaB kinase/nuclear factor kappaB-dependent insulin-like growth factor 2 (Igf2) expression regulates synapse formation and spine maturation via Igf2 receptor signaling. J Neurosci 32, 5688-5703.
Martin-Montanez E, Millon C, Boraldi F, Garcia-Guirado F, Pedraza C, Lara E, Santin LJ, Pavia J and Garcia-Fernandez M (2017) IGF-II promotes neuroprotection and neuroplasticity recovery in a long-lasting model of oxidative damage induced by glucocorticoids. Redox Biol 13, 69-81.
Martin-Montanez E, Pavia J, Santin LJ, Boraldi F, Estivill-Torrus G, Aguirre JA and Garcia-Fernandez M (2014) Involvement of IGF-II receptors in the antioxidant and neuroprotective effects of IGF-II on adult cortical neuronal cultures. Biochem Biophys Acta 1842, 1041-1051.
Wilhelm CJ, Hashimoto JG, Roberts ML, Sonmez MK and Wiren KM (2014) Understanding the addiction cycle: a complex biology with distinct contributions of genotype vs. sex at each stage. Neuroscience 279, 168-186.
Hashimoto JG and Wiren KM (2008) Neurotoxic consequences of chronic alcohol withdrawal: expression profiling reveals importance of gender over withdrawal severity. Neuropsychopharmacology 33, 1084-1096.
Wojcik SM, Tantra M, Stepniak B, Man KN, Muller-Ribbe K, Begemann M, Ju A, Papiol S, Ronnenberg A, Gurvich A et al. (2013) Genetic markers of a Munc13 protein family member, BAIAP3, are gender specifically associated with anxiety and benzodiazepine abuse in mice and humans. Mol Med 19, 135-148.
Heyer A, Hasselblatt M, von Ahsen N, Hafner H, Siren AL and Ehrenreich H (2005) In vitro gender differences in neuronal survival on hypoxia and in 17beta-estradiol-mediated neuroprotection. J Cereb Blood Flow Metab 25, 427-430.
Lieb K, Andrae J, Reisert I and Pilgrim C (1995) Neurotoxicity of dopamine and protective effects of the NMDA receptor antagonist AP-5 differ between male and female dopaminergic neurons. Exp Neurol 134, 222-229.
Villa A, Gelosa P, Castiglioni L, Cimino M, Rizzi N, Pepe G, Lolli F, Marcello E, Sironi L, Vegeto E et al. (2018) Sex-specific features of microglia from adult mice. Cell Rep 23, 3501-3511.
His W (1868) Untersuchungen über die erste Anlage des Wirbeltierleibes. Die erste Entwicklung des Hühnchens im Ei. Vogel, Leipzig.
Kaltschmidt B, Kaltschmidt C and Widera D (2012) Adult craniofacial stem cells: sources and relation to the neural crest. Stem Cell Rev 8, 658-671.
Huang X and Saint-Jeannet JP (2004) Induction of the neural crest and the opportunities of life on the edge. Dev Biol 275, 1-11.
Dupin E and Sommer L (2012) Neural crest progenitors and stem cells: from early development to adulthood. Dev Biol 366, 83-95.
Etchevers HC, Dupin E and Le Douarin NM (2019) The diverse neural crest: from embryology to human pathology. Development 146.
Burns AJ and Douarin NM (1998) The sacral neural crest contributes neurons and glia to the post-umbilical gut: spatiotemporal analysis of the development of the enteric nervous system. Development 125, 4335-4347.
Shakhova O and Sommer L (2008). Neural crest-derived stem cells. In StemBook (Gage F and Watt F, eds.), pp. 2-3. Harvard Stem Cell Institute, Cambridge, MA.
Faure S, McKey J, Sagnol S and de Santa Barbara P (2015) Enteric neural crest cells regulate vertebrate stomach patterning and differentiation. Development 142, 331-342.
Rios AC, Serralbo O, Salgado D and Marcelle C (2011) Neural crest regulates myogenesis through the transient activation of NOTCH. Nature 473, 532-535.
Clewes O, Narytnyk A, Gillinder KR, Loughney AD, Murdoch AP and Sieber-Blum M (2011) Human epidermal neural crest stem cells (hEPI-NCSC)-characterization and directed differentiation into osteocytes and melanocytes. Stem Cell Rev 7, 799-814.
Dupin E and Coelho-Aguiar JM (2013) Isolation and differentiation properties of neural crest stem cells. Cytometry A 83, 38-47.
Widera D, Grimm WD, Moebius JM, Mikenberg I, Piechaczek C, Gassmann G, Wolff NA, Thevenod F, Kaltschmidt C and Kaltschmidt B (2007) Highly efficient neural differentiation of human somatic stem cells, isolated by minimally invasive periodontal surgery. Stem Cells Dev 16, 447-460.
Delorme B, Nivet E, Gaillard J, Haupl T, Ringe J, Deveze A, Magnan J, Sohier J, Khrestchatisky M, Roman FS et al. (2010) The human nose harbors a niche of olfactory ectomesenchymal stem cells displaying neurogenic and osteogenic properties. Stem Cells Dev 19, 853-866.
Hauser S, Widera D, Qunneis F, Muller J, Zander C, Greiner J, Strauss C, Luningschror P, Heimann P, Schwarze H et al. (2012) Isolation of novel multipotent neural crest-derived stem cells from adult human inferior turbinate. Stem Cells Dev 21, 742-756.
Schurmann M, Brotzmann V, Butow M, Greiner J, Hoving A, Kaltschmidt C, Kaltschmidt B and Sudhoff H (2018) Identification of a novel high yielding source of multipotent adult human neural crest-derived stem cells. Stem Cell Rev Rep 14, 277-285.
Greiner JF, Gottschalk M, Fokin N, Buker B, Kaltschmidt BP, Dreyer A, Vordemvenne T, Kaltschmidt C, Hutten A and Kaltschmidt B (2019) Natural and synthetic nanopores directing osteogenic differentiation of human stem cells. Nanomedicine 17, 319-328.
Greiner JF, Hauser S, Widera D, Muller J, Qunneis F, Zander C, Martin I, Mallah J, Schuetzmann D, Prante C et al. (2011) Efficient animal-serum free 3D cultivation method for adult human neural crest-derived stem cell therapeutics. Eur Cell Mater 22, 403-419.
Müller J, Ossig C, Greiner JF, Hauser S, Fauser M, Widera D, Kaltschmidt C, Storch A and Kaltschmidt B (2015) Intrastriatal transplantation of adult human neural crest-derived stem cells improves functional outcome in parkinsonian rats. Stem Cells Transl Med 4, 31-43.
Toma JG, Akhavan M, Fernandes KJ, Barnabe-Heider F, Sadikot A, Kaplan DR and Miller FD (2001) Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat Cell Biol 3, 778-784.
Greiner JF, Grunwald LM, Muller J, Sudhoff H, Widera D, Kaltschmidt C and Kaltschmidt B (2014) Culture bag systems for clinical applications of adult human neural crest-derived stem cells. Stem Cell Res Ther 5, 34.
Hofemeier AD, Hachmeister H, Pilger C, Schurmann M, Greiner JF, Nolte L, Sudhoff H, Kaltschmidt C, Huser T and Kaltschmidt B (2016) Label-free nonlinear optical microscopy detects early markers for osteogenic differentiation of human stem cells. Sci Rep 6, 26716.
Schurmann M, Wolff A, Widera D, Hauser S, Heimann P, Hutten A, Kaltschmidt C and Kaltschmidt B (2014) Interaction of adult human neural crest-derived stem cells with a nanoporous titanium surface is sufficient to induce their osteogenic differentiation. Stem Cell Res 13, 98-110.
Bolande RP (1974) The neurocristopathies: a unifying concept of disease arising in neural crest maldevelopment. Hum Pathol 5, 409-429.
Howard TD, Paznekas WA, Green ED, Chiang LC, Ma N, Ortiz de Luna RI, Garcia Delgado C, Gonzalez-Ramos M, Kline AD and Jabs EW (1997) Mutations in TWIST, a basic helix-loop-helix transcription factor, in Saethre-Chotzen syndrome. Nat Genet 15, 36-41.
Sandell L (2014) Chapter 9 - Neural Crest Cells in Ear Development. In Neural Crest Cells (Trainor PA, ed), pp. 167-187. Academic Press, Boston.
Stoetzel C, Riehm S, Bennouna Greene V, Pelletier V, Vigneron J, Leheup B, Marion V, Helle S, Danse JM, Thibault C et al. (2009) Confirmation of TFAP2A gene involvement in branchio-oculo-facial syndrome (BOFS) and report of temporal bone anomalies. Am J Med Genet A 149A, 2141-2146.
Tekin M, Sirmaci A, Yuksel-Konuk B, Fitoz S and Sennaroglu L (2009) A complex TFAP2A allele is associated with branchio-oculo-facial syndrome and inner ear malformation in a deaf child. Am J Med Genet A 149A, 427-430.
Dixon MJ (1996) Treacher Collins syndrome. Hum Mol Genet 5, 1391-1396.
Stockton DW, Das P, Goldenberg M, D'Souza RN and Patel PI (2000) Mutation of PAX9 is associated with oligodontia. Nat Genet 24, 18-19.
Wilkie AO and Morriss-Kay GM (2001) Genetics of craniofacial development and malformation. Nat Rev Genet 2, 458-468.
Amiel J, Sproat-Emison E, Garcia-Barcelo M, Lantieri F, Burzynski G, Borrego S, Pelet A, Arnold S, Miao X, Griseri P et al. (2008) Hirschsprung disease, associated syndromes and genetics: a review. J Med Genet 45, 1-14.
Jiang Q, Liu F, Miao C, Li Q, Zhang Z, Xiao P, Su L, Yu K, Chen X, Zhang F et al. (2018) RET somatic mutations are underrecognized in Hirschsprung disease. Genet Med 20, 770-777.
Blitshteyn S, Crook JE and Jaeckle KA (2008) Is there an association between meningioma and hormone replacement therapy? J Clin Oncol 26, 279-282.
Andersen L, Friis S, Hallas J, Ravn P, Schrøder HD and Gaist D (2013) Hormone replacement therapy increases the risk of cranial meningioma. Eur J Cancer 49, 3303-3310.
Shpargel KB, Starmer J, Wang C, Ge K and Magnuson T (2017) UTX-guided neural crest function underlies craniofacial features of Kabuki syndrome. Proc Natl Acad Sci USA 114, E9046.
Bao AM and Swaab DF (2010) Sex differences in the brain, behavior, and neuropsychiatric disorders. Neuroscientist 16, 550-565.
Schwarz JM and Bilbo SD (2012) Sex, glia, and development: interactions in health and disease. Horm Behav 62, 243-253.
Reif A, Fritzen S, Finger M, Strobel A, Lauer M, Schmitt A and Lesch KP (2006) Neural stem cell proliferation is decreased in schizophrenia, but not in depression. Mol Psychiatry 11, 514-522.
Bonaguidi MA, Wheeler MA, Shapiro JS, Stadel RP, Sun GJ, Ming GL and Song H (2011) In vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics. Cell 145, 1142-1155.
Zhou J and Parada LF (2012) PTEN signaling in autism spectrum disorders. Curr Opin Neurobiol 22, 873-879.
Ghosh AK, Majumder M, Steele R, White RA and Ray RB (2001) A novel 16-kilodalton cellular protein physically interacts with and antagonizes the functional activity of c-myc promoter-binding protein 1. Mol Cell Biol 21, 655-662.
Superti-Furga A, Bonafe L and Rimoin DL (2001) Molecular-pathogenetic classification of genetic disorders of the skeleton. Am J Med Genet 106, 282-293.
Ngan ES, Garcia-Barcelo MM, Yip BH, Poon HC, Lau ST, Kwok CK, Sat E, Sham MH, Wong KK, Wainwright BJ, et al. (2011) Hedgehog/Notch-induced premature gliogenesis represents a new disease mechanism for Hirschsprung disease in mice and humans. J Clin Invest 121, 3467-3478.