Inducible deletion of epidermal Dicer and Drosha reveals multiple functions for miRNAs in postnatal skin

Development

Volumn 139, Issue 8, 2012, Pages 1405-1416

  Teta, Monica ^a   Choi, Yeon Sook ^a   Okegbe, Tishina ^a   Wong, Gabrielle ^a   Tam, Oliver H ^b   Chong, Mark M W ^c,f   Seykora, John T ^a   Nagy, Andras ^d   Littman, Dan R ^c   Andl, Thomas ^e   Millar, Sarah E ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d MOUNT SINAI HOSPITAL   (Canada)

^e VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^f WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

Dicer (Dicer1); Drosha; Epidermis; Hair follicle; miRNA; Mouse; Skin

Indexed keywords

CRE RECOMBINASE; DICER; ESTERASE; GENOMIC DNA; MICRORNA; PROTEIN DROSHA; UNCLASSIFIED DRUG;

ALLELE; ANIMAL CELL; APOPTOSIS; ARTICLE; BIODEGRADATION; BIOGENESIS; CELL DEATH; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DNA DAMAGE; DNA RECOMBINATION; DOWN REGULATION; EPIDERMIS; EPITHELIUM CELL; EXON; GENE DELETION; HAIR FOLLICLE; HAIR GROWTH; HISTOPATHOLOGY; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INFLAMMATION; MOUSE; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; RNA PROCESSING; SKIN; SKIN EPITHELIUM; STRUCTURE ANALYSIS; TRANSCRIPTION REGULATION; UPREGULATION;

ANIMALS; CROSSES, GENETIC; DEAD-BOX RNA HELICASES; EPIDERMIS; GENE DELETION; HAIR FOLLICLE; MICE; MICRORNAS; MICROSCOPY, FLUORESCENCE; PHENOTYPE; RIBONUCLEASE III; SIGNAL TRANSDUCTION; SKIN; STEM CELLS; WOUND HEALING;

MAMMALIA;

EID: 84858859031     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.070920     Document Type: Article

References (74)

1. Andl, T., Ahn, K., Kairo, A., Chu, E. Y., Wine-Lee, L., Reddy, S. T., Croft, N. J., Cebra-Thomas, J. A., Metzger, D., Chambon, P. et al. (2004). Epithelial Bmpr1a regulates differentiation and proliferation in postnatal hair follicles and is essential for tooth development. Development 131, 2257-2268.
2. Andl, T., Murchison, E. P., Liu, F., Zhang, Y., Yunta-Gonzalez, M., Tobias, J. W., Andl, C. D., Seykora, J. T., Hannon, G. J. and Millar, S. E. (2006). The miRNA-processing enzyme dicer is essential for the morphogenesis and maintenance of hair follicles. Curr. Biol. 16, 1041-1049.
3. Antonini, D., Russo, M. T., De Rosa, L., Gorrese, M., Del Vecchio, L. and Missero, C. (2010). Transcriptional repression of miR-34 family contributes to p63-mediated cell cycle progression in epidermal cells. J. Invest. Dermatol. 130, 1249-1257.
4. Baek, D., Villen, J., Shin, C., Camargo, F. D., Gygi, S. P. and Bartel, D. P. (2008). The impact of microRNAs on protein output. Nature 455, 64-71.
5. Biton, M., Levin, A., Slyper, M., Alkalay, I., Horwitz, E., Mor, H., Kredo-Russo, S., Avnit-Sagi, T., Cojocaru, G., Zreik, F. et al. (2011). Epithelial microRNAs regulate gut mucosal immunity via epithelium-T cell crosstalk. Nat. Immunol. 12, 239-246.
6. Blanpain, C. and Fuchs, E. (2009). Epidermal homeostasis: a balancing act of stem cells in the skin. Nat. Rev. Mol. Cell Biol. 10, 207-217.
7. Cheloufi, S., Dos Santos, C. O., Chong, M. M. and Hannon, G. J. (2010). A dicer-independent miRNA biogenesis pathway that requires Ago catalysis. Nature 465, 584-589.
8. Chong, M. M., Rasmussen, J. P., Rudensky, A. Y. and Littman, D. R. (2008). The RNase III enzyme Drosha is critical in T cells for preventing lethal inflammatory disease. J. Exp. Med. 205, 2005-2017.
9. Chong, M. M., Zhang, G., Cheloufi, S., Neubert, T. A., Hannon, G. J. and Littman, D. R. (2010). Canonical and alternate functions of the micro RNA biogenesis machinery. Genes Dev. 24, 1951-1960.
10. Cifuentes, D., Xue, H., Taylor, D. W., Patnode, H., Mishima, Y., Cheloufi, S., Ma, E., Mane, S., Hannon, G. J., Lawson, N. D. et al. (2010). A novel miRNA processing pathway independent of Dicer requires Argonaute2 catalytic activity. Science 328, 1694-1698.
11. Cotsarelis, G., Sun, T. T. and Lavker, R. M. (1990). Label-retaining cells reside in the bulge area of pilosebaceous unit: implications for follicular stem cells, hair cycle, and skin carcinogenesis. Cell 61, 1329-1337.
12. Dar, A. A., Majid, S., de Semir, D., Nosrati, M., Bezrookove, V. and Kashani-Sabet, M. (2011). MiRNA-205 suppresses melanoma cell proliferation and induces senescence via regulation of E2F1 protein. J. Biol. Chem. 286, 16606-16614.
13. DeGregori, J. (2002). The genetics of the E2F family of transcription factors: shared functions and unique roles. Biochim. Biophys. Acta 1602, 131-150.
14. Degregori, J. (2011). A new role for E2F1 in DNA repair: all for the greater good. Cell Cycle 10, 1716.
15. Demehri, S. and Kopan, R. (2009). Notch signaling in bulge stem cells is not required for selection of hair follicle fate. Development 136, 891-896.
16. Demehri, S., Liu, Z., Lee, J., Lin, M. H., Crosby, S. D., Roberts, C. J., Grigsby, P. W., Miner, J. H., Farr, A. G. and Kopan, R. (2008). Notch-deficient skin induces a lethal systemic B-lymphoproliferative disorder by secreting TSLP, a sentinel for epidermal integrity. PLoS Biol. 6, e123.
17. Demehri, S., Morimoto, M., Holtzman, M. J. and Kopan, R. (2009a). Skinderived TSLP triggers progression from epidermal-barrier defects to asthma. PLoS Biol. 7, e1000067.
18. Demehri, S., Turkoz, A. and Kopan, R. (2009b). Epidermal Notch1 loss promotes skin tumorigenesis by impacting the stromal microenvironment. Cancer Cell 16, 55-66.
19. Djuranovic, S., Nahvi, A. and Green, R. (2011). A parsimonious model for gene regulation by miRNAs. Science 331, 550-553.
20. Festa, E., Fretz, J., Berry, R., Schmidt, B., Rodeheffer, M., Horowitz, M. and Horsley, V. (2011). Adipocyte lineage cells contribute to the skin stem cell niche to drive hair cycling. Cell 146, 761-771.
21. Fuchs, E. (2007). Scratching the surface of skin development. Nature 445, 834-842.
22. Gregory, P. A., Bert, A. G., Paterson, E. L., Barry, S. C., Tsykin, A., Farshid, G., Vadas, M. A., Khew-Goodall, Y. and Goodall, G. J. (2008). The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat. Cell Biol. 10, 593-601.
23. He, L., He, X., Lim, L. P., de Stanchina, E., Xuan, Z., Liang, Y., Xue, W., Zender, L., Magnus, J., Ridzon, D. et al. (2007). A microRNA component of the p53 tumour suppressor network. Nature 447, 1130-1134.
24. Hebert, J. M., Rosenquist, T., Gotz, J. and Martin, G. R. (1994). FGF5 as a regulator of the hair growth cycle: evidence from targeted and spontaneous mutations. Cell 78, 1017-1025.
25. Hendrickson, D. G., Hogan, D. J., McCullough, H. L., Myers, J. W., Herschlag, D., Ferrell, J. E. and Brown, P. O. (2009). Concordant regulation of translation and mRNA abundance for hundreds of targets of a human microRNA. PLoS Biol. 7, e1000238.
26. Hener, P., Friedmann, L., Metzger, D., Chambon, P. and Li, M. (2011). Aggravated TSLP-induced atopic dermatitis in mice lacking dicer in adult skin keratinocytes. J. Invest. Dermatol. 131, 2324-2327.
27. Hildebrand, J., Rutze, M., Walz, N., Gallinat, S., Wenck, H., Deppert, W., Grundhoff, A. and Knott, A. (2011). A comprehensive analysis of microRNA expression during human keratinocyte differentiation in vitro and in vivo. J. Invest. Dermatol. 131, 20-29.
28. Hu, H. and Gatti, R. A. (2011). MicroRNAs: new players in the DNA damage response. J. Mol. Cell. Biol. 3, 151-158.
29. Hu, H., Du, L., Nagabayashi, G., Seeger, R. C. and Gatti, R. A. (2010). ATM is down-regulated by N-Myc-regulated microRNA-421. Proc. Natl. Acad. Sci. USA 107, 1506-1511.
30. Ito, M., Liu, Y., Yang, Z., Nguyen, J., Liang, F., Morris, R. J. and Cotsarelis, G. (2005). Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis. Nat. Med. 11, 1351-1354.
31. Kaufman, C. K., Zhou, P., Pasolli, H. A., Rendl, M., Bolotin, D., Lim, K. C., Dai, X., Alegre, M. L. and Fuchs, E. (2003). GATA-3: an unexpected regulator of cell lineage determination in skin. Genes Dev. 17, 2108-2122.
32. Lal, A., Pan, Y., Navarro, F., Dykxhoorn, D. M., Moreau, L., Meire, E., Bentwich, Z., Lieberman, J. and Chowdhury, D. (2009). MiR-24-mediated downregulation of H2AX suppresses DNA repair in terminally differentiated blood cells. Nat. Struct. Mol. Biol. 16, 492-498.
33. LeBoeuf, M., Terrell, A., Trivedi, S., Sinha, S., Epstein, J. A., Olson, E. N., Morrisey, E. E. and Millar, S. E. (2010). Hdac1 and Hdac2 act redundantly to control p63 and p53 functions in epidermal progenitor cells. Dev. Cell 19, 807-818.
34. Lee, J., Basak, J. M., Demehri, S. and Kopan, R. (2007). Bi-compartmental communication contributes to the opposite proliferative behavior of Notch1-deficient hair follicle and epidermal keratinocytes. Development 134, 2795-2806.
35. Lena, A. M., Shalom-Feuerstein, R., Rivetti di Val Cervo, P., Aberdam, D., Knight, R. A., Melino, G. and Candi, E. (2008). MiR-203 represses 'stemness' by repressing DeltaNp63. Cell Death Differ. 15, 1187-1195.
36. Leung, A. K. and Sharp, P. A. (2010). MicroRNA functions in stress responses. Mol. Cell 40, 205-215.
37. Lewis, B. P., Burge, C. B. and Bartel, D. P. (2005). Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15-20.
38. Liu, Y. and Liu, Q. (2011). ATM signals miRNA biogenesis through KSRP. Mol. Cell 41, 367-368.
39. Lynch, M. H., O'Guin, W. M., Hardy, C., Mak, L. and Sun, T. T. (1986). Acidic and basic hair/nail ("hard") keratins: their colocalization in upper cortical and cuticle cells of the human hair follicle and their relationship to "soft" keratins. J. Cell Biol. 103, 2593-2606.
40. Majid, S., Saini, S., Dar, A. A., Hirata, H., Shahryari, V., Tanaka, Y., Yamamura, S., Ueno, K., Zaman, M. S., Singh, K. et al. (2011). MicroRNA-205 inhibits Src-mediated oncogenic pathways in renal cancer. Cancer Res. 71, 2611-2621.
41. Mardaryev, A. N., Ahmed, M. I., Vlahov, N. V., Fessing, M. Y., Gill, J. H., Sharov, A. A. and Botchkareva, N. V. (2010). Micro-RNA-31 controls hair cycle-associated changes in gene expression programs of the skin and hair follicle. FASEB J. 24, 3869-3881.
42. Matsumoto, T., Jiang, J., Kiguchi, K., Ruffino, L., Carbajal, S., Beltran, L., Bol, D. K., Rosenberg, M. P. and DiGiovanni, J. (2003). Targeted expression of c-Src in epidermal basal cells leads to enhanced skin tumor promotion, malignant progression, and metastasis. Cancer Res. 63, 4819-4828.
43. Millar, S. E. (2002). Molecular mechanisms regulating hair follicle development. J. Invest. Dermatol. 118, 216-225.
44. Murchison, E. P., Partridge, J. F., Tam, O. H., Cheloufi, S. and Hannon, G. J. (2005). Characterization of Dicer-deficient murine embryonic stem cells. Proc. Natl. Acad. Sci. USA 102, 12135-12140.
45. Nowak, J. A., Polak, L., Pasolli, H. A. and Fuchs, E. (2008). Hair follicle stem cells are specified and function in early skin morphogenesis. Cell Stem Cell 3, 33-43.
46. O'Guin, W. M., Sun, T. T. and Manabe, M. (1992). Interaction of trichohyalin with intermediate filaments: three immunologically defined stages of trichohyalin maturation. J. Invest. Dermatol. 98, 24-32.
47. Oliver, R. F. and Jahoda, C. A. (1988). Dermal-epidermal interactions. Clin. Dermatol. 6, 74-82.
48. Pan, Y., Lin, M. H., Tian, X., Cheng, H. T., Gridley, T., Shen, J. and Kopan, R. (2004). Gamma-secretase functions through Notch signaling to maintain skin appendages but is not required for their patterning or initial morphogenesis. Dev. Cell 7, 731-743.
49. Paterson, E. L., Kolesnikoff, N., Gregory, P. A., Bert, A. G., Khew-Goodall, Y. and Goodall, G. J. (2008). The microRNA-200 family regulates epithelial to mesenchymal transition. Scientific World Journal 8, 901-904.
50. Peters, E. M., Maurer, M., Botchkarev, V. A., Jensen, K., Welker, P., Scott, G. A. and Paus, R. (2003). Kit is expressed by epithelial cells in vivo. J. Invest. Dermatol. 121, 976-984.
51. Pierce, A. M., Fisher, S. M., Conti, C. J. and Johnson, D. G. (1998). Deregulated expression of E2F1 induces hyperplasia and cooperates with ras in skin tumor development. Oncogene 16, 1267-1276.
52. Plikus, M. V., Mayer, J. A., de la Cruz, D., Baker, R. E., Maini, P. K., Maxson, R. and Chuong, C. M. (2008). Cyclic dermal BMP signalling regulates stem cell activation during hair regeneration. Nature 451, 340-344.
53. Rendl, M., Lewis, L. and Fuchs, E. (2005). Molecular dissection of mesenchymalepithelial interactions in the hair follicle. PLoS Biol. 3, e331.
54. Ruby, J. G., Jan, C. H. and Bartel, D. P. (2007). Intronic microRNA precursors that bypass Drosha processing. Nature 448, 83-86.
55. Ryan, D. G., Oliveira-Fernandes, M. and Lavker, R. M. (2006). MicroRNAs of the mammalian eye display distinct and overlapping tissue specificity. Mol. Vis. 12, 1175-1184.
56. Selbach, M., Schwanhausser, B., Thierfelder, N., Fang, Z., Khanin, R. and Rajewsky, N. (2008). Widespread changes in protein synthesis induced by microRNAs. Nature 455, 58-63.
57. Shenoy, A. and Blelloch, R. (2009). Genomic analysis suggests that mRNA destabilization by the microprocessor is specialized for the auto-regulation of Dgcr8. PLoS ONE 4, e6971.
58. Suzuki, H. I., Yamagata, K., Sugimoto, K., Iwamoto, T., Kato, S. and Miyazono, K. (2009). Modulation of microRNA processing by p53. Nature 460, 529-533.
59. Tam, O. H., Aravin, A. A., Stein, P., Girard, A., Murchison, E. P., Cheloufi, S., Hodges, E., Anger, M., Sachidanandam, R., Schultz, R. M. et al. (2008). Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 453, 534-538.
60. Teta, M., Rankin, M. M., Long, S. Y., Stein, G. M. and Kushner, J. A. (2007). Growth and regeneration of adult beta cells does not involve specialized progenitors. Dev. Cell 12, 817-826.
61. Vauclair, S., Nicolas, M., Barrandon, Y. and Radtke, F. (2005). Notch1 is essential for postnatal hair follicle development and homeostasis. Dev. Biol. 284, 184-193.
62. Watanabe, T., Totoki, Y., Toyoda, A., Kaneda, M., Kuramochi-Miyagawa, S., Obata, Y., Chiba, H., Kohara, Y., Kono, T., Nakano, T. et al. (2008). Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 453, 539-543.
63. Wu, H., Xu, H., Miraglia, L. J. and Crooke, S. T. (2000). Human RNase III is a 160-kDa protein involved in preribosomal RNA processing. J. Biol. Chem. 275, 36957-36965.
64. Xin, H. B., Deng, K. Y., Shui, B., Qu, S., Sun, Q., Lee, J., Greene, K. S., Wilson, J., Yu, Y., Feldman, M. et al. (2005). Gene trap and gene inversion methods for conditional gene inactivation in the mouse. Nucleic Acids Res. 33, e14.
65. Xu, N., Brodin, P., Wei, T., Meisgen, F., Eidsmo, L., Nagy, N., Kemeny, L., Stahle, M., Sonkoly, E. and Pivarcsi, A. (2011). MiR-125b, a MicroRNA downregulated in psoriasis, modulates keratinocyte proliferation by targeting FGFR2. J. Invest. Dermatol. 131, 1521-1529.
66. Yagi, R., Waguri, S., Sumikawa, Y., Nada, S., Oneyama, C., Itami, S., Schmedt, C., Uchiyama, Y. and Okada, M. (2007). C-terminal Src kinase controls development and maintenance of mouse squamous epithelia. EMBO J. 26, 1234-1244.
67. Yi, R., O'Carroll, D., Pasolli, H. A., Zhang, Z., Dietrich, F. S., Tarakhovsky, A. and Fuchs, E. (2006). Morphogenesis in skin is governed by discrete sets of differentially expressed microRNAs. Nat. Genet. 38, 356-362.
68. Yi, R., Poy, M. N., Stoffel, M. and Fuchs, E. (2008). A skin microRNA promotes differentiation by repressing 'stemness'. Nature 452, 225-229.
69. Yi, R., Pasolli, H. A., Landthaler, M., Hafner, M., Ojo, T., Sheridan, R., Sander, C., O'Carroll, D., Stoffel, M., Tuschl, T. et al. (2009). DGCR8-dependent microRNA biogenesis is essential for skin development. Proc. Natl. Acad. Sci. USA 106, 498-502.
70. Yu, J., Peng, H., Ruan, Q., Fatima, A., Getsios, S. and Lavker, R. M. (2010). MicroRNA-205 promotes keratinocyte migration via the lipid phosphatase SHIP2. FASEB J. 24, 3950-3959.
71. Zhang, L., Stokes, N., Polak, L. and Fuchs, E. (2011). Specific microRNAs are preferentially expressed by skin stem cells to balance self-renewal and early lineage commitment. Cell Stem Cell 8, 294-308.
72. Zhang, X., Wan, G., Berger, F. G., He, X. and Lu, X. (2011). The ATM kinase induces microRNA biogenesis in the DNA damage response. Mol. Cell 41, 371-383.
73. Zhang, Y., Andl, T., Yang, S. H., Teta, M., Liu, F., Seykora, J. T., Tobias, J. W., Piccolo, S., Schmidt-Ullrich, R., Nagy, A. et al. (2008). Activation of betacatenin signaling programs embryonic epidermis to hair follicle fate. Development 135, 2161-2172.
74. Zhang, Y., Tomann, P., Andl, T., Gallant, N. M., Huelsken, J., Jerchow, B., Birchmeier, W., Paus, R., Piccolo, S., Mikkola, M. L. et al. (2009). Reciprocal requirements for EDA/EDAR/NF-kappaB and Wnt/beta-catenin signaling pathways in hair follicle induction. Dev. Cell 17, 49-61.