Conditional Activin Receptor Type 1B (Acvr1b) Knockout Mice Reveal Hair Loss Abnormality

Journal of Investigative Dermatology

Volumn 131, Issue 5, 2011, Pages 1067-1076

  Qiu, Wanglong ^a   Li, Xiaojun ^a   Tang, Hongyan ^a   Huang, Alicia S ^a   Panteleyev, Andrey A ^b   Owens, David M ^a   Su, Gloria H ^a  

^a ICRC 1004 ^*  (United States)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN; ACTIVIN RECEPTOR 1; ACTIVIN RECEPTOR 1B; BONE MORPHOGENETIC PROTEIN; CYTOKERATIN 14; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ALOPECIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EPIDERMIS; EPITHELIUM CELL; FEMALE; HAIR CYCLE REENTRY; HAIR CYCLING; HAIR FOLLICLE; HAIR GROWTH; HAIR LOSS; HISTOPATHOLOGY; KNOCKOUT MOUSE; MORPHOGENESIS; MOUSE; NEWBORN; NONHUMAN; PHENOTYPE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SKIN EPITHELIUM; SKINFOLD THICKNESS; WILD TYPE;

EID: 79954677720     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/jid.2010.400     Document Type: Article

References (68)

1. Attisano L, Carcamo J, Ventura F et al. (1993) Identification of human activin and TGF beta type I receptors that form heteromeric kinase complexes with type II receptors. Cell 75:671-80 (Pubitemid 23346366)
2. Attisano L, Wrana JL, Montalvo E et al. (1996) Activation of signalling by the activin receptor complex. Mol Cell Biol 16:1066-73 (Pubitemid 26061678)
3. Ball EM, Risbridger GP (2001) Activins as regulators of branching morphogenesis. Dev Biol 238:1-12 (Pubitemid 32939282)
4. Bamberger C, Scharer A, Antsiferova M et al. (2005) Activin controls skin morphogenesis and wound repair predominantly via stromal cells and in a concentration-dependent manner via keratinocytes. Am J Pathol 167: 733-47 (Pubitemid 41216358)
5. Botchkarev VA, Botchkareva NV, Roth W et al. (1999) Noggin is a mesenchymally derived stimulator of hair-follicle induction. Nat Cell Biol 1:158-64 (Pubitemid 129656020)
6. Burdette JE, Jeruss JS, Kurley SJ et al. (2005) Activin A mediates growth inhibition and cell cycle arrest through Smads in human breast cancer cells. Cancer Res 65:7968-75 (Pubitemid 41297276)
7. Byrne C, Tainsky M, Fuchs E (1994) Programming gene expression in developing epidermis. Development 120:2369-83 (Pubitemid 24268813)
8. Chen Y, Mironova E, Whitaker LL et al. (2004) ALK4 functions as a receptor for multiple TGF beta-related ligands to regulate left-right axis determination and mesoderm induction in Xenopus. Dev Biol 268:280-94 (Pubitemid 38519844)
9. Cruise BA, Xu P, Hall AK (2004) Wounds increase activin in skin and a vasoactive neuropeptide in sensory ganglia. Dev Biol 271:1-10 (Pubitemid 38757770)
10. D'Abronzo FH, Swearingen B, Klibanski A et al. (1999) Mutational analysis of activin/transforming growth factor-beta type I and type II receptor kinases in human pituitary tumors. J Clin Endocrinol Metab 84:1716-21 (Pubitemid 30644282)
11. Danila DC, Zhang X, Zhou Y et al. (2002) Overexpression ofwild-typeactivin receptor alk4-1 restores activin antiproliferative effects in human pituitary tumor cells. J Clin Endocrinol Metab 87:4741-6 (Pubitemid 35247070)
12. Derynck R, Zhang Y, Feng XH (1998) Smads: transcriptional activators of TGF-beta responses. Cell95:737-40 (Pubitemid 29014453)
13. Ferguson CA, Tucker AS, Christensen L et al. (1998) Activin is an essential early mesenchymal signal in tooth development that is required for patterning of the murine dentition. Genes Dev 12:2636-49 (Pubitemid 28406964)
14. Ferguson CA, Tucker AS, Heikinheimo K et al. (2001) The role of effectors of the activin signalling pathway, activin receptors IIA and IIB, and Smad2, in patterning of tooth development. Development 128:4605-13 (Pubitemid 33130440)
15. Foitzik K, Paus R, Doetschman T et al. (1999) The TGF-beta2 isoform is both a required and sufficient inducer of murine hair foll icle morphogenesis. Dev Biol 212:278-89 (Pubitemid 29387936)
16. Fuchs E, Raghavan S (2002) Getting under the skin of epidermal morphogen-esis. Nat Rev Genet 3:199-209
17. Gu Z, Nomura M, Simpson BB et al. (1998) Thetype I activin receptor ActRIB is required for egg cylinder organization and gastrulation in the mouse. Genes Dev 12:844-57 (Pubitemid 28150885)
18. Han G, Li AG, Liang YY et al. (2006) Smad7-induced beta-catenin degradation alters epidermal appendage development [see comment]. Develop Cell 11:301-12 (Pubitemid 44283940)
19. Heldin CH, Miyazono K, Ten Dijke P (1997) TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 390:465-71 (Pubitemid 28013118)
20. Hempen PM, Zhang L, Bansal RK et al. (2003) Evidence of selection for clones having genetic inactivation of the activin A type II receptor (ACVR2) gene in gastrointestinal cancers. Cancer Res 63:994-9 (Pubitemid 36278430)
21. Hubner G, Brauchle M, Gregor M et al. (1997) Activin A: a novel player and inflammatory marker in inflammatory bowel disease? Lab Invest 77:311-8 (Pubitemid 27465593)
22. Ito M, Kizawa K, Hamada K et al. (2004) Hair foll icle stem cells in the lower bulge form the secondary germ, a biochemically distinct but functionally equivalent progenitor cell population, at the termination of catagen. Differentiation 72:548-57 (Pubitemid 41702109)
23. Jernvall J, Thesleff I (2000) Reiterative signaling and patterning during mammalian tooth morphogenesis. Mech Dev 92:19-29 (Pubitemid 30125959)
24. Jonkers J, Meuwissen R, van der Gulden H et al. (2001) Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer. Nat Genet 29:418-25 (Pubitemid 34326692)
25. Kim SK, Hebrok M, Li E et al. (2000) Activin receptor patterning of foregut organogenesis. Genes Dev 14:1866-71 (Pubitemid 30639520)
26. Kobielak K, Pasolli HA, Alonso L et al. (2003) Defining BMP functions in the hair follicle by conditional ablation of BMP receptor IA. J Cell Biol 163:609-23 (Pubitemid 37429873)
27. Ling N, Ying SY, Ueno N et al. (1986) Pituitary FSH is released by a heterodimer of the beta-subunits from the two forms of inhibin. Nature 321:779-82 (Pubitemid 16077905)
28. Lynch MH, O'Guin WM, Hardy C et al. (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 103:2593-606 (Pubitemid 17008006)
29. Massague J (1996) TGFbeta signaling: receptors, transducers, and Mad proteins. Cell 85:947-50
30. Massague J (1998) TGF-beta signal transduction. Annu Rev Biochem 67:753-91
31. Mathews LS, Vale WW, Kintner CR (1992) Cloning of a second type of activin receptor and functional characterization in Xenopus embryos. Science 255:1702-5
32. Matzuk MM, Finegold MJ, Su JG et al. (1992) Alpha-inhibin is a tumour-suppressor gene with gonadal specificity in mice. Nature 360:313-9 (Pubitemid 23000668)
33. Matzuk MM, Kumar TR, Bradley A (1995a) Different phenotypes for mice deficient in either activins or activin receptor type II. Nature 374:356-60
34. Matzuk MM, Kumar TR, Vassalli A et al. (1995b) Functional analysis of activins during mammalian development. Nature 374:354-6
35. Matzuk MM, Lu N, Vogel H et al. (1995c) Multiple defects and perinatal death in mice deficient in follistatin. Nature 374:360-3
36. McDowall M, Edwards NM, Jahoda CA et al. (2008) The role of activins and follistatins in skin and hair follic le development and function. Cytokine Growth Factor Rev 19:415-26
37. Merino R, Macias D, Ganan Y et al. (1999) Control of digit formation by activin signalling. Development 126:2161-70 (Pubitemid 29271701)
38. Millar SE (2002) Molecular mechanisms regulating hair follicle development. J Invest Dermatol 118:216-25 (Pubitemid 34158473)
39. Munz B, Smola H, Engelhardt F et al. (1999) Overexpression of activin A in the skin of transgenic mice reveals new activities of activin in epidermal morphogenesis, dermal fibrosis and wound repair. EMBOJ 18:5205-15 (Pubitemid 29465571)
40. Nakamura M, Matzuk MM, Gerstmayer B et al. (2003) Control of pelage hair follicle development and cycling by complex interactions between follistatin and activin. FASEBJ 17:497-9
41. O'Guin WM, Sun TT, Manabe M (1992) Interaction of trichohyalin with intermediate filaments: three immunologically defined stages of tricho-hyalin maturation. J Invest Dermatol 98:24-32
42. Ohyama M, Terunuma A, Tock CL et al. (2006) Characterization and isolation of stem cell-enriched human hair follicle bulge cells. J Clin Invest 116:249-60 (Pubitemid 43121810)
43. Owens P, Han G, Li AG et al. (2008) The role of Smads in skin development. J Invest Dermatol 128:783-90 (Pubitemid 351374283)
44. Panopoulou E, Murphy C, Rasmussen H et al. (2005) Activin A suppresses neuroblastoma xenograft tumor growth via antimitotic and antiangio-genic mechanisms. Cancer Res 65:1877-86 (Pubitemid 40478616)
45. Piek E, Heldin CH, Ten Dijke P (1999) Specificity, diversity, and regulation in TGF-beta superfamily signaling. FASEB J 13:2105-24
46. Qiao W, Li AG, Owens P et al. (2006) Hair follicle defects and squamous cell carcinoma formation in Smad4 conditional knockout mouse skin. Oncogene 25:207-17 (Pubitemid 43083682)
47. Risbridger GP, Schmitt JF, Robertson DM (2001) Activins and inhibins in endocrine and other tumors. Endocr Rev22:836-58 (Pubitemid 34214298)
48. Roberts VJ, Barth SL (1994) Expression of messenger ribonucleic acids encoding the inhibin/activin system during mid-and late-gestation rat embryogenesis. Endocrinology 134:914-23 (Pubitemid 24057241)
49. Rossi MR, Ionov Y, Bakin AV et al. (2005) Truncating mutations in the ACVR2 gene attenuates activin signaling in prostate cancer cells. Cancer Genet Cytogenet 163:123-9 (Pubitemid 41758453)
50. Smith JC, Price BM, Van Nimmen K et al. (1990) Identification of a potent Xenopus mesoderm-inducing factor as a homologue of activin A. Nature 345:729-31
51. Song J, Oh SP, Schrewe H et al. (1999) The type II activin receptors are essential for egg cylinder growth, gastrulation, and rostral head development in mice. Dev Biol 213:157-69 (Pubitemid 29409953)
52. Su GH, Bansal R, Murphy KM et al. (2001) ACVR1B (ALK4, activin receptor type 1B) gene mutations in pancreatic carcinoma. Proc Natl Acad Sci USA 98:3254-7 (Pubitemid 32220832)
53. Thesleff I, Keranen S, Jernvall J (2001) Enamel knots as signaling centers linking tooth morphogenesis and odontoblast differentiation. Adv Dent Res 15:14-8
54. Thesleff I, Wang XP, Suomalainen M (2007) Regulation of epithelial stem cells in tooth regeneration. C R Biol 330:561-4 (Pubitemid 47040685)
55. Thompson TB, Cook RW, Chapman SC et al. (2004) Beta A versus beta B: is it merely a matter of expression? Mol Cell Endocrinol 225:9-17 (Pubitemid 39297049)
56. Thomsen G, Woolf T, Whitman M et al. (1990) Activins are expressed early in Xenopus embryogenesis and can induce axial mesoderm and anterior structures. Cell 63:485-93
57. Vassalli A, Matzuk MM, Gardner HA et al. (1994) Activin/inhibin beta B subunit gene disruption leads to defects in eyelid development and female reproduction. Genes Dev8:414-27
58. Vassar R, Fuchs E (1991) Transgenic mice provide new insights into the role of TGF-alpha during epidermal development and differentiation. Genes Dev 5:714-27 (Pubitemid 21905990)
59. Verschueren K, Dewulf N, Goumans MJ et al. (1995) Expression of type I and type IB receptors for activin in midgestation mouse embryos suggests distinct functions in organogenesis. Mech Dev 52:109-23
60. Wang X, Zinkel S, Polonsky K et al. (1997) Transgenic studies with a keratin promoter-driven growth hormone transgene: prospects for gene therapy. Proc Natl Acad Sci USA 94:219-26 (Pubitemid 27027190)
61. Wang XP, Suomalainen M, Felszeghy S et al. (2007) An integrated gene regulatory network controls stem cell proliferation in teeth. PLoS Biol 5:e159
62. Wang Z, Wong P, Langbein L et al. (2003) Type II epithelial keratin 6hf (K6hf) is expressed in the companion layer, matrix, and medulla in anagen-stage hair foll icles. J Invest Dermatol 121:1276-82 (Pubitemid 38005473)
63. Wang XP, Suomalainen M, Jorgez CJ et al. (2004) Follistatin regulates enamel patterning in mouse incisors by asymmetrically inhibiting BMP signaling and ameloblast differentiation. Dev Cell 7:719-30 (Pubitemid 39462692)
64. Wilson C, Cotsarelis G, Wei ZG et al. (1994) Cells within the bulge region of mouse hair follicle transiently proliferate during early anagen: hetero-geneity and functional differences of various hair cycles. Differentiation 55:127-36 (Pubitemid 24051747)
65. Woodruff TK (1998) Regulation of cellular and system function by activin. Biochem Pharmacol 55:953-63 (Pubitemid 28167717)
66. Yeo C, Whitman M (2001) Nodal signals to Smads through Cripto-dependent and Cripto-independent mechanisms. Mol Cell 7:949-57 (Pubitemid 32525742)
67. Zhou P, Byrne C, Jacobs J et al. (1995) Lymphoid enhancer factor 1 directs hair follicle patterning and epithelial cell fate. Genes Dev 9:700-13
68. Zimmers TA, Davies MV, Koniaris LG et al. (2002) Induction of cachexia in mice by systemically administered myostatin. Science 296:1486-8 (Pubitemid 34553097)