ΔNp63 regulates stem cell dynamics in the Mammalian olfactory epithelium

Journal of Neuroscience

Volumn 31, Issue 24, 2011, Pages 8748-8759

  Packard, Adam ^a,b   Schnittke, Nikolai ^a,b   Romano, Rose Anne ^c   Sinha, Satrajit ^c   Schwob, James E ^a,b  

^a TUFTS UNIVERSITY   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HES 1; TRANSCRIPTION FACTOR MASH1; TRANSCRIPTION FACTOR P63; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; 5 ETHYNYLDEOXYURIDINE; 5-ETHYNYL-2'-DEOXYURIDINE; ASCL1 PROTEIN, MOUSE; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; DEOXYURIDINE; DRUG DERIVATIVE; GREEN FLUORESCENT PROTEIN; ISOPROTEIN; PGP9.5 PROTEIN, MOUSE; PHOSPHOPROTEIN; SOX2 PROTEIN, MOUSE; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR SOX; TRP63 PROTEIN, MOUSE; UBIQUITIN THIOLESTERASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL REGENERATION; CELL STRUCTURE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EMBRYO CELL; GENE SILENCING; GLOBOSE BASAL CELL; HORIZONTAL BASAL CELL; MULTIPOTENT STEM CELL; NEURAL STEM CELL; NONHUMAN; OLFACTORY EPITHELIUM; OLFACTORY PROGENITORS OF THE EMBRYONIC PLACODE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; AGE; ANALYSIS OF VARIANCE; ANIMAL; ANIMAL EMBRYO; C57BL MOUSE; CELL DIVISION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METHODOLOGY; MOUSE; NEWBORN; NONLINEAR SYSTEM; PHYSIOLOGY; SPRAGUE DAWLEY RAT; STEM CELL; TRANSGENIC MOUSE; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELL DIVISION; DEOXYURIDINE; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, ELECTRON, TRANSMISSION; NONLINEAR DYNAMICS; OLFACTORY MUCOSA; PHOSPHOPROTEINS; PROTEIN ISOFORMS; RATS; RATS, SPRAGUE-DAWLEY; SOXB1 TRANSCRIPTION FACTORS; STEM CELLS; TRANS-ACTIVATORS; UBIQUITIN THIOLESTERASE;

EID: 79959286263     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0681-11.2011     Document Type: Article

References (51)

1. Candi E, Rufini A, Terrinoni A, Dinsdale D, Ranalli M, Paradisi A, De Laurenzi V, Spagnoli LG, Catani MV, Ramadan S, Knight RA, Melino G (2006) Differential roles of p63 isoforms in epidermal development: selective genetic complementation in p63 null mice. Cell Death Differ 13:1037-1047.
2. Candi E, Dinsdale D, Rufini A, Salomoni P, Knight RA, Mueller M, Krammer PH, Melino G (2007) TAp63 and DeltaNp63 in cancer and epidermal development. Cell Cycle 6:274-285.
3. Carlén M, Meletis K, Goritz C, Darsalia V, Evergren E, Tanigaki K, Amendola M, Barnabe-Heider F, Yeung MS, Naldini L, Honjo T, Kokaia Z, Shuplia-kov O, Cassidy RM, Lindvall O, Frisen J (2009) Forebrain ependymal cells are Notch-dependent and generate neuroblasts and astrocytes after stroke. Nat Neurosci 12:259-267.
4. Carroll DK, Carroll JS, Leong CO, Cheng F, Brown M, Mills AA, Brugge JS, Ellisen LW (2006) p63 regulates an adhesion programme and cell survival in epithelial cells. Nat Cell Biol 8:551-561.
5. Carter LA, MacDonald JL, Roskams AJ (2004) Olfactory horizontal basal cells demonstrate a conserved multipotent progenitor phenotype. J Neu-rosci 24:5670-5683.
6. Cau E, Gradwohl G, Casarosa S, Kageyama R, Guillemot F (2000) Hes genes regulate sequential stages of neurogenesis in the olfactory epithelium. Development 127:2323-2332.
7. Cau E, Casarosa S, Guillemot F (2002) Mash1 and Ngn1 control distinct stepsof determination and differentiationin the olfactory sensory neuron lineage. Development 129:1871-1880.
8. Chen X, Fang H, Schwob JE (2004) Multipotency of purified, transplanted globose basal cells in olfactory epithelium. J Comp Neurol 469:457-474.
9. Crum CP, McKeon FD (2010) p63 in epithelial survival, germ cell surveillance, and neoplasia. Annu Rev Pathol 5:349-371.
10. Delorme B, Nivet E, Gaillard J, Haupl T, Ringe J, Deveze A, Magnan J, Sohier J, Khrestchatisky M, Roman FS, Charbord P, Sensebe L, Layrolle P, Feron F (2010) The human nose harborsanicheofolfactory ectomesenchymal stem cells displaying neurogenic and osteogenic properties. Stem Cells Dev 19:853-866.
11. Ghioni P, Bolognese F, Duijf PH, Van Bokhoven H, Mantovani R, Guerrini L (2002) Complex transcriptional effects of p63 isoforms: identification of novel activation and repression domains. Mol Cell Biol 22:8659-8668.
12. Goldstein BJ, Fang H, Youngentob SL, Schwob JE (1998) Transplantation of multipotent progenitors from the adult olfactory epithelium. Neurore-port 9:1611-1617.
13. Graziadei PP, Graziadei GA (1979) Neurogenesis and neuron regeneration in the olfactory system of mammals. I. Morphological aspects of differentiation and structural organization of the olfactory sensory neurons. J Neurocytol 8:1-18.
14. Guo Z, Packard A, Krolewski RC, Harris MT, Manglapus GL, Schwob JE (2010) Expression of Pax6 and Sox2 in adult olfactory epithelium. J Comp Neurol 518:4395-4418.
15. Holbrook EH, Szumowski KE, Schwob JE (1995) An immunochemical, ul-trastructural, and developmental characterization of the horizontal basal cells of rat olfactory epithelium. J Comp Neurol 363:129-146.
16. Holbrook EH, Leopold DA, Schwob JE (2005) Abnormalities of axon growth in human olfactory mucosa. Laryngoscope 115:2144-2154.
17. Huard JM, Youngentob SL, Goldstein BJ, Luskin MB, Schwob JE (1998) Adult olfactory epithelium contains multipotent progenitors that give rise to neurons and non-neural cells. J Comp Neurol 400:469-486.
18. Ito M, Yang Z, Andl T, Cui C, Kim N, Millar SE, Cotsarelis G (2007) Wnt-dependent de novo hair follicle regeneration in adult mouse skin after wounding. Nature 447:316-320.
19. Ito T, Udaka N, Yazawa T, Okudela K, Hayashi H, Sudo T, Guillemot F, Kageyama R, Kitamura H (2000) Basic helix-loop-helix transcription factors regulate the neuroendocrine differentiation offetal mouse pulmonary epithelium. Development 127:3913-3921.
20. Iwai N, Zhou Z, Roop DR, Behringer RR (2008) Horizontal basal cells are multipotent progenitors in normal and injured adult olfactory epithelium. Stem Cells 26:1298-1306.
21. Jacobs WB, Govoni G, Ho D, Atwal JK, Barnabe-Heider F, Keyes WM, Mills AA, Miller FD, Kaplan DR (2005) p63 is an essential proapoptotic protein during neural development. Neuron 48:743-756.
22. Jang W, Youngentob SL, Schwob JE (2003) Globose basal cells are required for reconstitution of olfactory epithelium after methyl bromide lesion. J Comp Neurol 460:123-140.
23. Keyes WM, Pecoraro M, Aranda V, Vernersson-Lindahl E, Li W, Vogel H, Guo X, Garcia EL, Michurina TV, Enikolopov G, Muthuswamy SK, Mills AA (2011) DeltaNp63alpha is an oncogene that targets chromatin re-modeler Lsh to drive skin stem cell proliferation and tumorigenesis. Cell Stem Cell 8:164-176.
24. Kikuchi T, Ichimiya S, Kojima T, Crisa L, Koshiba S, Tonooka A, Kondo N, Van Der Saag PT, Yokoyama S, Sato N (2004) Expression profiles and functional implications ofp53-like transcription factorsinthymic epithelial cell subtypes. Int Immunol 16:831-841.
25. Koster MI, Dai D, Marinari B, Sano Y, Costanzo A, Karin M, Roop DR (2007) p63 induces key target genes required for epidermal morphogenesis. Proc Natl Acad Sci USA 104:3255-3260.
26. Kubilus JK, Linsenmayer TF (2010) Developmental corneal innervation: interactions between nerves and specialized apical corneal epithelial cells. Invest Ophthalmol Vis Sci 51:782-789.
27. Largent BL, Sosnowski RG, Reed RR (1993) Directed expression of an on-cogene to the olfactory neuronal lineage in transgenic mice. J Neurosci 13:300-312.
28. Laurikkala J, Mikkola ML, James M, Tummers M, Mills AA, Thesleff I (2006) p63 regulates multiple signalling pathways required for ectodermal or-ganogenesis and differentiation. Development 133:1553-1563.
29. Lena AM, Shalom-Feuerstein R, Rivetti di Val Cervo P, Aberdam D, Knight RA, Melino G, Candi E (2008) miR-203 represses 'stemness' by repressing DeltaNp63. Cell Death Differ 15:1187-1195.
30. Leung CT, Coulombe PA, Reed RR (2007) Contribution of olfactory neural stem cells to tissue maintenance and regeneration. Nat Neurosci 10:720-726.
31. Manglapus GL, Youngentob SL, Schwob JE (2004) Expression patterns of basic helix-loop-helix transcription factors define subsets of olfactory progenitor cells. J Comp Neurol 479:216-233.
32. McKeon F, Melino G (2007) Fogof war: the emerging p53 family. Cell Cycle 6:229-232.
33. Mills AA, Zheng B, Wang XJ, Vogel H, Roop DR, Bradley A (1999) p63 is a p53 homologue required for limb and epidermal morphogenesis. Nature 398:708-713.
34. Nakamuta N, Kobayashi S (2007) Expression of p63 in the mouse ovary. J Reprod Dev 53:691-697.
35. Nguyen BC, Lefort K, Mandinova A, Antonini D, Devgan V, Della Gatta G, Koster MI, Zhang Z, Wang J, Tommasi di Vignano A, Kitajewski J, Chi-orino G, Roop DR, Missero C, Dotto GP (2006) Cross-regulation between Notch and p63 in keratinocyte commitment to differentiation. Genes Dev 20:1028-1042.
36. Noszczyk BH, Majewski ST (2001) p63 expression during normal cutaneous wound healing in humans. Plast Reconstr Surg 108:1242-1247.
37. Romano RA, Birkaya B, Sinha S (2006) Defining the regulatory elements in the proximal promoter of DeltaNp63 in keratinocytes: potential roles for Sp1/Sp3, NF-Y, and p63. J Invest Dermatol 126:1469-1479.
38. Romano RA, Ortt K, Birkaya B, Smalley K, Sinha S (2009) An active role of the DeltaN isoform of p63 in regulating basal keratin genes K5 and K14 and directing epidermal cell fate. PLoS One 4:e5623.
39. Romano RA, Smalley K, Liu S, Sinha S (2010) Abnormal hair follicle development and altered cell fate of follicular keratinocytes in transgenic mice expressing DeltaNp63alpha. Development 137:1431-1439.
40. Schwob JE, Youngentob SL, Mezza RC (1995) Reconstitution of the rat olfactory epithelium after methyl bromide-induced lesion. J Comp Neurol 359:15-37.
41. Su X, Paris M, Gi YJ, Tsai KY, Cho MS, Lin YL, Biernaskie JA, Sinha S, Prives C, Pevny LH, Miller FD, Flores ER (2009) TAp63 prevents premature aging by promoting adult stem cell maintenance. Cell Stem Cell 5:64-75.
42. Suh EK, Yang A, Kettenbach A, Bamberger C, Michaelis AH, Zhu Z, Elvin JA, Bronson RT, Crum CP, McKeon F (2006) p63 protects the female germ line during meiotic arrest. Nature 444:624-628.
43. Suzuki Y, Takeda M (1991) Keratins in the developing olfactory epithelia. Brain Res Dev Brain Res 59:171-178.
44. Thépot A, Hautefeuille A, Cros MP, Abedi-Ardekani B, Petre A, Damour O, Krutovskikh V, Hainaut P (2010) Intraepithelial p63-dependent expression of distinct components of cell adhesion complexes in normal esoph-ageal mucosa and squamous cell carcinoma. Int J Cancer 127:2051-2062.
45. Tomé M, Lindsay SL, Riddell JS, Barnett SC (2009) Identification of non-epithelial multipotent cellsinthe embryonic olfactory mucosa. Stem Cells 27:2196-2208.
46. Wildner H, Muller T, Cho SH, Brohl D, Cepko CL, Guillemot F, Birchmeier C (2006) DILA neurons in the dorsal spinal cord are the product of terminal and non-terminal asymmetric progenitor cell divisions, and require Mash1 for their development. Development 133:2105-2113.
47. Yalcin-Ozuysal O, Fiche M, Guitierrez M, Wagner KU, Raffoul W, Brisken C (2010) Antagonistic roles of Notch and p63 in controlling mammary epithelial cell fates. Cell Death Differ 17:1600 -1612.
48. Yang A, Kaghad M, Wang Y, Gillett E, Fleming MD, Dotsch V, Andrews NC, Caput D, McKeon F (1998) p63, a p53 homolog at 3q27-29, encodes multiple products with transactivating, death-inducing, and dominant-negative activities. Mol Cell 2:305-316.
49. Yang A, Schweitzer R, Sun D, Kaghad M, Walker N, Bronson RT, Tabin C, Sharpe A, Caput D, Crum C, McKeon F (1999) p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development. Nature 398:714-718.
50. Yang A, Zhu Z, Kapranov P, McKeon F, Church GM, Gingeras TR, Struhl K (2006) Relationships between p63 binding, DNA sequence, transcription activity, and biological function in human cells. Mol Cell 24:593-602.
51. Yi R, Poy MN, Stoffel M, Fuchs E (2008) A skin microRNA promotes differentiation by repressing 'stemness'. Nature 452:225-229.