Cytomegalovirus induces abnormal chondrogenesis and osteogenesis during embryonic mandibular development

BMC Developmental Biology

Volumn 8, Issue , 2008, Pages

  Jaskoll, Tina ^a   Abichaker, George ^a   Sedghizadeh, Parish P ^a   Bringas Jr , Pablo ^a   Melnick, Michael ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; SMAD7 PROTEIN; SHH PROTEIN, MOUSE; SONIC HEDGEHOG PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BRANCHIAL ARCH; CELL DIFFERENTIATION; CHONDROGENESIS; CONTROLLED STUDY; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; DEVELOPMENTAL DISORDER; DISEASE PREDISPOSITION; EMBRYO; FEMALE; IN VITRO STUDY; MESENCHYME CELL; MICROGNATHIA; MOUSE; NEURAL CREST; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; SALIVARY GLAND; VIRUS INFECTION; ANIMAL; BETAHERPESVIRINAE; EMBRYO (ANATOMY); GENE EXPRESSION REGULATION; GENETICS; MANDIBLE; PATHOPHYSIOLOGY; PREGNANCY; PRENATAL DEVELOPMENT; SIGNAL TRANSDUCTION;

CYTOMEGALOVIRUS;

ANIMALS; CHONDROGENESIS; CYTOMEGALOVIRUS INFECTIONS; EMBRYO, MAMMALIAN; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; MANDIBLE; MICE; MUROMEGALOVIRUS; NF-KAPPA B; OSTEOGENESIS; PREGNANCY; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 42549109410     PISSN: None     EISSN: 1471213X     Source Type: Journal    
DOI: 10.1186/1471-213X-8-33     Document Type: Article

References (69)

1. The epidemiology and prevention of congenital cytomegalovirus infection and disease: activities of the Centers for Disease Control and Prevention Workgroup. Ross DS Dollard SC Victor M Sumartojo E Cannon MJ, J Womens Health (Larchmt) 2006 15 224 229 16620180
2. Centers for Disease Control and Prevention. http://www.cdc.gov/cmv
3. Cytomegalovirus. Pass RF, Fields Virology Volume 2, Fourth Edition Philadelphia, Lippincott Williams & Wilkins, Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE, 2001 2675 2705
4. Pathogenesis of murine cytomegalovirus infection. Krmpotic A Bubic I Polic B Lucin P Jonjic S, Microbes Infect 2003 5 1263 1277 10.1016/j.micinf. 2003.09.007 14623023
5. Demonstration of developmental anomalies in mouse fetuses by transfer of murine cytomegalovirus DNA-injected eggs to surrogate mothers. Baskar JF Furnari B Huang ES, J Infect Dis 1993 167 1288 1295 8388900
6. Early-stage developmental abnormalities induced by murine cytomegalovirus. Baskar JF Peacock J Sulik KK Huang ES, J Infect Dis 1987 155 661 666 3029242
7. Murine cytomegalovirus-induced congenital defects and fetal maldevelopment. Baskar JF Stanat SC Sulik KK Huang ES, J Infect Dis 1983 148 836 843 6313819
8. Growth retardation and microcephaly induced in mice by placental infection with murine cytomegalovirus. Li RY Tsutsui Y, Teratology 2000 62 79 85 10.1002/1096-9926(200008)62:2<79::AID-TERA3>3.0.CO;2-S 10931504
9. Developmental disorders of the mouse brain induced by murine cytomegalovirus: animal models for congenital cytomegalovirus infection. Tsutsui Y, Pathol Int 1995 45 91 102 7742931
10. Cytomegalovirus inhibition of embryonic mouse tooth development: a model of the human amelogenesis imperfect phenocopy. T Jaskoll G Abichaker N Jangaard P Bringas Jr M Melnick, Arch Oral Biol 2007 53 405 415 10.1016/j.archoralbio. 2007.11.014
11. Cytomegalovirus-induced embryopathology: Mouse submandibular salivary gland epithelial-mesenchymal ontogeny as a model. Melnick M Mocarski ES Abichaker G Huang J Jaskoll T, BMC Dev Biol 2006 6 42 16959038 10.1186/1471-213X-6-42
12. The role of the neural crest in patterning of avian cranial skeletal, connective, and muscle tissues. Noden DM, Dev Biol 1983 96 144 165 10.1016/0012-1606(83)90318-4 6825950
13. Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Chai Y Jiang X Ito Y Bringas P Jr Han J Rowitch DH Soriano P McMahon AP Sucov HM, Development 2000 127 1671 1679 10725243
14. The Neural Crest. Le Douarin NM Kalcheim C, New York, Cambridge University Press 2nd 1999
15. Histochemical and immunohistochemical analysis of the mechanism of calcification of Meckel's cartilage during mandible development in rodents. Ishizeki K Saito H Shinagawa T Fujiwara N Nawa T, J Anat 1999 194 265 277 10337959 10.1046/j.1469-7580.1999.19420265.x
16. All for one and one for all: condensation and the initiation of skeletal development. Hall BK Miyake T, BioEssays 2000 22 138 147 10.1002/(SICI)1521- 1878(200002)22:2<138::AID-BIES5>3.0.CO;2-4 10655033
17. The growth and morphogenesis of the early mouse mandible: a quantitative analysis. Ramaesh T Bard JB, J Anat 2003 203 213 222 12924821 10.1046/j.1469-7580.2003.00210.x
18. Meckel's cartilage differentiation is dependent on hedgehog signaling. M Melnick D Witcher P Bringas Jr P Carlsson T Jaskoll, Cells Tissues Organs 2005 179 146 157 10.1159/000085950 16046861
19. Receptor-Regulated and inhibitory Smads are critical in regulating transforming growth factor β-mediated Meckel's cartilage development. Ito Y Bringas P Mogharei A Zhao J Deng C Chai Y, Developmental Dynamics 2002 224 69 78 10.1002/dvdy.10088 11984875
20. Recent advances in craniofacial morphogenesis. Chai Y Maxson RE Jr, Dev Dyn 2006 235 2353 2375 10.1002/dvdy.20833 16680722
21. Role of Meckel's cartilage in the development and growth of the rat mandible. Bhaskar SN Weinmann JP Schour I, J Dent Res 1953 32 398 410 13061679
22. Contribution of Meckel's cartilage to ossification of the mandible in mice. Frommer J Margolies MR, J Dent Res 1971 50 1260 1267 5285785
23. Resorption of calcified cartilage as seen in Meckel's cartilage of rats. Savostin-Asling I Asling CW, Anat Rec 1973 176 345 359 10.1002/ar.1091760310 4716419
24. Expression and roles of connective tissue growth factor in Meckel's cartilage development. Shimo T Kanyama M Wu C Sugito H Billings PC Abrams WR Rosenbloom J Iwamoto M Pacifici M Koyama E, Dev Dyn 2004 231 136 147 10.1002/dvdy.20109 15305294
25. gp130 is important for the normal morphogenesis of Meckel's cartilage and subsequent mandibular development. Choi JW Kim JT Park JH Park EK Kim SY Kwon TG Kim EC Shin HI, Exp Mol Med 2007 39 295 303 17603283
26. Schemes of zonation in the mandibular condyle. Beresford WA, Am J Orthod 1975 68 189 195 10.1016/0002-9416(75)90207-9 1056706
27. FGF10/FGFR2b signaling plays essential roles during in vivo embryonic submandibular salivary gland morphogenesis. Jaskoll T Abichaker G Witcher D Sala FG Bellusci S Hajihosseini MK Melnick M, BMC Dev Biol 2005 5 11 22 15972105 10.1186/1471-213X-5-11
28. The nature of endochondral ossification in the mandibular condyle of the mouse. Silbermann M Frommer J, Anat Rec 1972 172 659 667 10.1002/ar.1091720406 5027572
29. Cellular stages in cartilage formation as revealed by morphometry, radioautography and type II collagen immunostaining of the mandibular condyle from weanling rats. Luder HU Leblond CP von der Mark K, Am J Anat 1988 182 197 214 10.1002/aja.1001820302 3213819
30. An in situ hybridization and histochemical study of development and postnatal changes of mouse mandibular angular cartilage compared with condylar cartilage. Shibata S Fujimori T Yamashita Y, J Med Dent Sci 2006 53 41 50 16722144
31. A histological study of the developing condylar cartilage of the fetal mouse mandible using coronal sections. Shibata S Suzuki S Tengan T Ishii M Kuroda T, Arch Oral Biol 1996 41 47 54 10.1016/0003-9969(95)00105-0 8833590
32. Temporomandibular joint formation and condyle growth require Indian hedgehog signaling. Shibukawa Y Young B Wu C Yamada S Long F Pacifici M Koyama E, Dev Dyn 2007 236 426 434 10.1002/dvdy.21036 17191253
33. Morphogenesis of the medial region of the developing mandible is regulated by multiple signaling pathways. Mina M, Cells Tissues Organs 2001 169 295 301 10.1159/000047894 11455126
34. Regulation of mandibular growth and morphogenesis. Mina M, Crit Rev Oral Biol Med 2001 12 276 300 11603502
35. Divide, accumulate, differentiate: cell condensation in skeletal development revisited. Hall BK Miyake T, Int J Dev Biol 1995 39 881 893 8901191
36. Spatiotemporal patterns of fibronectin distribution during embryonic development. II. Chick branchial arches. Jaskoll T Melnick M MacDougall M Brownell AG Slavkin HC, J Craniofac Genet Dev Biol 1981 1 203 212 7040441
37. The functional genomic response of developing embryonic submandibular glands to NF-kappa B inhibition. Melnick M Chen H Min Zhou Y Jaskoll T, BMC Dev Biol 2001 1 15 33 11716784 10.1186/1471-213X-1-15
38. Requirement of NF-kappaB/Rel for the development of hair follicles and other epidermal appendices. Schmidt-Ullrich R Aebischer T Hülsken J Birchmeier W Klemm U Scheidereit C, Development 2001 128 3843 3853 11585809
39. A dual role for Ikk alpha in tooth development. Ohazama A Hu Y Schmidt-Ullrich R Cao Y Scheidereit C Karin M Sharpe PT, Dev Cell 2004 6 219 227 10.1016/S1534-5807(04)00024-3 14960276
40. The Ectoctodysplasin and NFkappaB signaling pathways in odontogenesis. JM Courtney J Blackburn PT Sharpe, Arch Oral Bio 2005 50 159 163 10.1016/j.archoralbio.2004.11.019
41. Neutrality of the canonical NF-kappaB-dependent pathway for human and murine cytomegalovirus transcription and replication in vitro. Benedict CA Angulo A Patterson G Ha S Huang H Messerle M Ware CF Ghazal P, J Virol 2004 78 741 750 14694106 10.1128/JVI.78.2.741-750.2004
42. Activation of the NF-kappaB pathway in human cytomegalovirus-infected cells is necessary for efficient transactivation of the major immediate-early promoter. DeMeritt IB Milford LE Yurochko AD, J Virol 2004 78 4498 4507 15078930 10.1128/JVI.78.9.4498-4507.2004
43. Prolonged activation of NF-kappaB by human cytomegalovirus promotes efficient viral replication and late gene expression. DeMeritt IB Podduturi JP Tilley AM Nogalski MT Yurochko AD, Virology 2006 346 15 31 10.1016/j.virol.2005. 09.065 16303162
44. RelB-p50 NF-kappa B complexes are selectively induced by cytomegalovirus immediate-early protein 1: differential regulation of Bcl-x(L) promoter activity by NF-kappa B family members. Jiang HY Petrovas C Sonenshein GE, J Virol 2002 76 5737 5747 11992002 10.1128/JVI.76.11.5737-5747.2002
45. Induction of the RelB NF-kappaB subunit by the cytomegalovirus IE1 protein is mediated via Jun kinase and c-Jun/Fra-2 AP-1 complexes. Wang X Sonenshein GE, J Virol 2005 79 95 105 15596805 10.1128/JVI.79.1.95-105.2005
46. Human cytomegalovirus upregulates NF-kappa B activity by transactivating the NF-kappa B p105/p50 and p65 promoters. Yurochko AD Kowalik TF Huong SM Huang ES, J Virol 1995 69 5391 5400 7636984
47. Induction of the transcription factor Sp1 during human cytomegalovirus infection mediates upregulation of the p65 and p105/p50 NF-kappaB promoters. Yurochko AD Mayo MW Poma EE Baldwin AS Jr Huang ES, J Virol 1997 71 4638 4648 9151857
48. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Chiang C Litingtung Y Lee E Young KE Corden JL Westphal H Beachy PA, Nature 1996 383 407 413 10.1038/383407a0 8837770
49. Hedgehog signaling in the neural crest cells regulates the patterning and growth of facial primordia. Jeong J Mao J Tenzen T Kottmann AH McMahon AP, Genes Dev 2004 18 937 951 15107405 10.1101/gad.1190304
50. Distinct roles for Hedgehog and canonical Wnt signaling in specification, differentiation and maintenance of osteoblast progenitors. Rodda SJ McMahon AP, Development 2006 133 3231 3244 10.1242/dev.02480 16854976
51. Sonic Hedgehog promotes the development of multipotent neural crest progenitors endowed with both mesenchymal and neural potentials. Calloni GW Glavieux-Pardanaud C Le Douarin NM Dupin E, Proc Natl Acad Sci U S A 2007 104 19879 19884 10.1073/pnas.0708806104 18077420
52. Nuclear factor-κB contributes to hedgehog signaling pathway activation through sonic hedgehog induction in pancreatic cancer. Nakashima H Nakamura M Yamaguchi H Yamanaka N Akiyoshi T Koga K Yamaguchi K Tsuneyoshi M Tanaka M Katano M, Cancer Res 2006 66 7041 7049 10.1158/0008-5472.CAN-05-4588 16849549
53. Conditional inactivation of Tgfbr2 in cranial neural crest causes cleft palate and calvaria defects. Ito Y Yeo JY Chytil A Han J Bringas P Nakajima A Schuler CF Moses HL Chai Y, Development 2003 130 5269 5280 10.1242/dev.00708 12975342
54. The role of TGF-beta signaling in regulating chondrogenesis and osteogenesis during mandibular development. Oka K Oka S Sasaki T Ito Y Bringas P Jr Nonaka K Chai Y, Dev Biol 2007 303 391 404 17204263 10.1016/j.ydbio.2006.11. 025
55. TGFβ2 knockout mice have multiple developmental defects that are non-over-lapping with other TGFβ knockout phenotypes. Sanford LP Ormsby I Gittenberger-de Groot AC Sariola H Friedman R Boivin GP Cardell EI Doestschman T, Development 1997 124 2659 2670 9217007
56. A mechanism of suppression of TGF-beta/SMAD signaling by NF-κB/RelA. Bitzer M von Gersdorff G Liang D Dominguez-Rosales A Beg AA Rojkind M Böttinger EP, Genes Dev 2000 14 187 197 10652273
57. Smad7 mediates inhibition of Saos2 osteosarcoma cell differentiation by NFkappaB. Eliseev RA Schwarz EM Zuscik MJ O'Keefe RJ Drissi H Rosier RN, Exp Cell Res 2006 312 40 50 10.1016/j.yexcr.2005.09.016 16259979
58. Absence of IL-1 receptor antagonist impaired wound healing along with aberrant NF-kappaB activation and a reciprocal suppression of TGF-beta signal pathway. Ishida Y Kondo T Kimura A Matsushima K Mukaida N, J Immunol 2006 176 5598 5606 16622029
59. Sonic hedgehog regulates otic capsule chondrogenesis and inner ear development in the mouse embryo. Liu W Li G Chien JS Raft S Zhang H Chiang C Frenz DA, Dev Biol 2002 248 240 250 10.1006/dbio.2002.0733 12167401
60. Cellular interactions and signaling in cartilage development. DeLise AM Fischer L Tuan RS, Osteoarthritis Cartilage 2000 8 309 334 10.1053/joca.1999. 0306 10966838
61. Functions of NF-kappaB1 and NF-kappaB2 in immune cell biology. Beinke S Ley SC, Biochem J 2004 382 393 409 15214841 10.1042/BJ20040544
62. The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Bonizzi G Karin M, Trends Immunol 2004 25 280 288 10.1016/j.it.2004.03.008 15145317
63. Rel/NF-kappaB transcription factors: key mediators of B-cell activation. Gugasyan R Grumont R Grossmann M Nakamura Y Pohl T Nesic D Gerondakis S, Immunol Rev 2000 176 134 140 10.1034/j.1600-065X.2000.00615.x 11043773
64. NF-κB specifically activates BMP-2 gene expression in growth plate chondrocytes in vivo and in a chondrocyte cell line in vitro. Feng JQ Xing L Zhang JH Zhao M Horn D Chan J Boyce BF Harris SE Mundy GR Chen D, J Biol Chem 2003 278 29130 29135 10.1074/jbc.M212296200 12759356
65. Requirement for NF-κB in osteoclast and B-cell development. Franzoso G Carlson L Xing L Poljak L Shores EW Brown KD Leonardi A Tran T Boyce BF Siebenlist U, Genes Dev 1997 11 3482 3496 9407039 10.1101/gad.11.24.3482
66. Selective inhibition of NF-kappa B blocks osteoclastogenesis and prevents inflammatory bone destruction in vivo. Jimi E Aoki K Saito H D'Acquisto F May MJ Nakamura I Sudo T Kojima T Okamoto F Fukushima H Okabe K Ohya K Ghosh S, Nat Med 2004 10 617 624 10.1038/nm1054 15156202
67. TGF-β signaling and its functional significance in regulating the fate of cranial neural crest cells. Y Chai Y Ito J Han, Crit Rev Oral Biol Med 2003 14 78 88 12764071
68. Cytomegalovirus-encoded beta chemokine promotes monocyte-associated viremia in the host. Saederup N Lin YC Dairaghi DJ Schall TJ Mocarski ES, Proc Natl Acad Sci U S A 1999 96 10881 10886 10485920 10.1073/pnas.96.19.10881
69. Embryonic salivary gland branching morphogenesis. Jaskoll T Melnick M, Branching Morphogenesis Georgetown, TX, Landes Biosciences, JA Davis, 2004