Hoxa1 lineage tracing indicates a direct role for Hoxa1 in the development of the inner ear, the heart, and the third rhombomere

Developmental Biology

Volumn 341, Issue 2, 2010, Pages 499-509

  Makki, Nadja ^a   Capecchi, Mario R ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Heart; Hindbrain; Hoxa1; Inner ear

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HOXA1; UNCLASSIFIED DRUG; HOMEOBOX A1 PROTEIN; HOMEODOMAIN PROTEIN;

ABDUCENS NUCLEUS; ANIMAL TISSUE; ARTICLE; BRAIN STEM; CONTROLLED STUDY; DEVELOPMENTAL GENETICS; EMBRYO; EMBRYO DEVELOPMENT; FACIAL NERVE; GENE EXPRESSION; GENE FUNCTION; HEART DEVELOPMENT; INNER EAR; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL CREST CELL; NEUROMERE; NONHUMAN; PRIORITY JOURNAL; ANIMAL; HEART; METABOLISM; PRENATAL DEVELOPMENT;

MUS;

ANIMALS; BRAIN STEM; EAR, INNER; HEART; HOMEODOMAIN PROTEINS; MICE; TRANSCRIPTION FACTORS;

EID: 77952310728     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.02.014     Document Type: Article

References (64)

1. Alexander T., Nolte C., Krumlauf R. Hox genes and segmentation of the hindbrain and axial skeleton. Annu. Rev. Cell Dev. Biol. 2009, 25:431-456.
2. Arenkiel B.R., Gaufo G.O., Capecchi M.R. Hoxb1 neural crest preferentially form glia of the PNS. Dev. Dyn. 2003, 227:379-386.
3. Baker C.V., Bronner-Fraser M. Vertebrate cranial placodes: I. Embryonic induction. Dev. Biol. 2001, 232:1-61.
4. Baker C.V., Bronner-Fraser M., Le Douarin N.M., Teillet M.A. Early- and late-migrating cranial neural crest cell populations have equivalent developmental potential in vivo. Development 1997, 124:3077-3087.
5. Barlow L.A. Cranial nerve development: placodal neurons ride the crest. Curr. Biol. 2002, 12:R171-R173.
6. Barrow J.R., Stadler H.S., Capecchi M.R. Roles of Hoxa1 and Hoxa2 in patterning the early hindbrain of the mouse. Development 2000, 127:933-944.
7. Begbie J., Graham A. Integration between the epibranchial placodes and the hindbrain. Science 2001, 294:595-598.
8. Bok J., Chang W., Wu D.K. Patterning and morphogenesis of the vertebrate inner ear. Int. J. Dev. Biol. 2007, 51:521-533.
9. Bosley T.M., Salih M.A., Alorainy I.A., Oystreck D.T., Nester M., Abu-Amero K.K., Tischfield M.A., Engle E.C. Clinical characterization of the HOXA1 syndrome BSAS variant. Neurology 2007, 69:1245-1253.
10. Bosley T.M., Alorainy I.A., Salih M.A., Aldhalaan H.M., Abu-Amero K.K., Oystreck D.T., Tischfield M.A., Engle E.C., Erickson R.P. The clinical spectrum of homozygous HOXA1 mutations. Am. J. Med. Genet. A 2008, 146A:1235-1240.
11. Branda C.S., Dymecki S.M. Talking about a revolution: the impact of site-specific recombinases on genetic analyses in mice. Dev. Cell 2004, 6:7-28.
12. Britsch S., Goerich D.E., Riethmacher D., Peirano R.I., Rossner M., Nave K.A., Birchmeier C., Wegner M. The transcription factor Sox10 is a key regulator of peripheral glial development. Genes Dev. 2001, 15:66-78.
13. Brown C.B., Baldwin H.S. Neural crest contribution to the cardiovascular system. Adv. Exp. Med. Biol. 2006, 589:134-154.
14. Bruneau B.G., Logan M., Davis N., Levi T., Tabin C.J., Seidman J.G., Seidman C.E. Chamber-specific cardiac expression of Tbx5 and heart defects in Holt-Oram syndrome. Dev. Biol. 1999, 211:100-108.
15. Capecchi M.R. Hox genes and mammalian development. Cold Spring Harbor Symp. Quant. Biol. 1997, 62:273-281.
16. Champagnat J., Fortin G. Primordial respiratory-like rhythm generation in the vertebrate embryo. Trends Neurosci. 1997, 20:119-124.
17. Chisaka O., Musci T.S., Capecchi M.R. Developmental defects of the ear, cranial nerves and hindbrain resulting from targeted disruption of the mouse homeobox gene Hox-1.6. Nature 1992, 355:516-520.
18. Coutinho A.P., Borday C., Gilthorpe J., Jungbluth S., Champagnat J., Lumsden A., Fortin G. Induction of a parafacial rhythm generator by rhombomere 3 in the chick embryo. J. Neurosci. 2004, 24:9383-9390.
19. Danielian P.S., Muccino D., Rowitch D.H., Michael S.K., McMahon A.P. Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr. Biol. 1998, 8:1323-1326.
20. Forlani S., Lawson K.A., Deschamps J. Acquisition of Hox codes during gastrulation and axial elongation in the mouse embryo. Development 2003, 130:3807-3819.
21. Gavalas A., Studer M., Lumsden A., Rijli F.M., Krumlauf R., Chambon P. Hoxa1 and Hoxb1 synergize in patterning the hindbrain, cranial nerves and second pharyngeal arch. Development 1998, 125:1123-1136.
22. Gavalas A., Trainor P., Ariza-McNaughton L., Krumlauf R. Synergy between Hoxa1 and Hoxb1: the relationship between arch patterning and the generation of cranial neural crest. Development 2001, 128:3017-3027.
23. Godwin A.R., Stadler H.S., Nakamura K., Capecchi M.R. Detection of targeted GFP-Hox gene fusions during mouse embryogenesis. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:13042-13047.
24. Haldar M., Karan G., Tvrdik P., Capecchi M.R. Two cell lineages, myf5 and myf5-independent, participate in mouse skeletal myogenesis. Dev. Cell 2008, 14:437-445.
25. Hatch E.P., Noyes C.A., Wang X., Wright T.J., Mansour S.L. Fgf3 is required for dorsal patterning and morphogenesis of the inner ear epithelium. Development 2007, 134:3615-3625.
26. Helmbacher F., Pujades C., Desmarquet C., Frain M., Rijli F.M., Chambon P., Charnay P. Hoxa1 and Krox-20 synergize to control the development of rhombomere 3. Development 1998, 125:4739-4748.
27. Henrique D., Adam J., Myat A., Chitnis A., Lewis J., Ish-Horowicz D. Expression of a Delta homologue in prospective neurons in the chick. Nature 1995, 375:787-790.
28. Hogan B., Wright C. Developmental biology. The making of the ear. Nature 1992, 355:494-495.
29. Holve S., Friedman B., Hoyme H.E., Tarby T.J., Johnstone S.J., Erickson R.P., Clericuzio C.L., Cunniff C. Athabascan brainstem dysgenesis syndrome. Am. J. Med. Genet. A 2003, 120:169-173.
30. Iimura T., Pourquie O. Hox genes in time and space during vertebrate body formation. Dev. Growth Differ. 2007, 49:265-275.
31. Jepsen K., Hermanson O., Onami T.M., Gleiberman A.S., Lunyak V., McEvilly R.J., Kurokawa R., Kumar V., Liu F., Seto E., Hedrick S.M., Mandel G., Glass C.K., Rose D.W., Rosenfeld M.G. Combinatorial roles of the nuclear receptor corepressor in transcription and development. Cell 2000, 102:753-763.
32. Jiang Y., Tarzami S., Burch J.B., Evans T. Common role for each of the cGATA-4/5/6 genes in the regulation of cardiac morphogenesis. Dev. Genet. 1998, 22:263-277.
33. Jiang X., Rowitch D.H., Soriano P., McMahon A.P., Sucov H.M. Fate of the mammalian cardiac neural crest. Development 2000, 127:1607-1616.
34. Jostes B., Walther C., Gruss P. The murine paired box gene, Pax7, is expressed specifically during the development of the nervous and muscular system. Mech. Dev. 1990, 33:27-37.
35. Jukkola T., Trokovic R., Maj P., Lamberg A., Mankoo B., Pachnis V., Savilahti H., Partanen J. Meox1Cre: a mouse line expressing Cre recombinase in somitic mesoderm. Genesis 2005, 43:148-153.
36. Kiernan A.E., Pelling A.L., Leung K.K., Tang A.S., Bell D.M., Tease C., Lovell-Badge R., Steel K.P., Cheah K.S. Sox2 is required for sensory organ development in the mammalian inner ear. Nature 2005, 434:1031-1035.
37. Kirby M.L., Waldo K.L. Neural crest and cardiovascular patterning. Circ. Res. 1995, 77:211-215.
38. Kontges G., Lumsden A. Rhombencephalic neural crest segmentation is preserved throughout craniofacial ontogeny. Development 1996, 122:3229-3242.
39. Lufkin T., Dierich A., LeMeur M., Mark M., Chambon P. Disruption of the Hox-1.6 homeobox gene results in defects in a region corresponding to its rostral domain of expression. Cell 1991, 66:1105-1119.
40. Lumsden A., Keynes R. Segmental patterns of neuronal development in the chick hindbrain. Nature 1989, 337:424-428.
41. Lumsden A., Krumlauf R. Patterning the vertebrate neuraxis. Science 1996, 274:1109-1115.
42. Maka M., Stolt C.C., Wegner M. Identification of Sox8 as a modifier gene in a mouse model of Hirschsprung disease reveals underlying molecular defect. Dev. Biol. 2005, 277:155-169.
43. Mao X., Fujiwara Y., Chapdelaine A., Yang H., Orkin S.H. Activation of EGFP expression by Cre-mediated excision in a new ROSA26 reporter mouse strain. Blood 2001, 97:324-326.
44. Mark M., Lufkin T., Vonesch J.L., Ruberte E., Olivo J.C., Dolle P., Gorry P., Lumsden A., Chambon P. Two rhombomeres are altered in Hoxa-1 mutant mice. Development 1993, 119:319-338.
45. McClintock J.M., Jozefowicz C., Assimacopoulos S., Grove E.A., Louvi A., Prince V.E. Conserved expression of Hoxa1 in neurons at the ventral forebrain/midbrain boundary of vertebrates. Dev. Genes Evol. 2003, 213:399-406.
46. Mitchell P.J., Timmons P.M., Hebert J.M., Rigby P.W., Tjian R. Transcription factor AP-2 is expressed in neural crest cell lineages during mouse embryogenesis. Genes Dev. 1991, 5:105-119.
47. Morrison A.D. 1+1=r4 and much much more. Bioessays 1998, 20:794-797.
48. Morrison S.J., White P.M., Zock C., Anderson D.J. Prospective identification, isolation by flow cytometry, and in vivo self-renewal of multipotent mammalian neural crest stem cells. Cell 1999, 96:737-749.
49. Mujtaba T., Mayer-Proschel M., Rao M.S. A common neural progenitor for the CNS and PNS. Dev. Biol. 1998, 200:1-15.
50. Murphy P., Hill R.E. Expression of the mouse labial-like homeobox-containing genes, Hox 2.9 and Hox 1.6, during segmentation of the hindbrain. Development 1991, 111:61-74.
51. Ohyama T., Groves A.K. Generation of Pax2-Cre mice by modification of a Pax2 bacterial artificial chromosome. Genesis 2004, 38:195-199.
52. Pattyn A., Morin X., Cremer H., Goridis C., Brunet J.F. Expression and interactions of the two closely related homeobox genes Phox2a and Phox2b during neurogenesis. Development 1997, 124:4065-4075.
53. Rodriguez C.I., Buchholz F., Galloway J., Sequerra R., Kasper J., Ayala R., Stewart A.F., Dymecki S.M. High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP. Nat. Genet. 2000, 25:139-140.
54. Rossel M., Capecchi M.R. Mice mutant for both Hoxa1 and Hoxb1 show extensive remodeling of the hindbrain and defects in craniofacial development. Development 1999, 126:5027-5040.
55. Ryckebusch L., Wang Z., Bertrand N., Lin S.C., Chi X., Schwartz R., Zaffran S., Niederreither K. Retinoic acid deficiency alters second heart field formation. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:2913-2918.
56. Snider P., Olaopa M., Firulli A.B., Conway S.J. Cardiovascular development and the colonizing cardiac neural crest lineage. Sci. World J. 2007, 7:1090-1113.
57. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 1999, 21:70-71.
58. Srinivas S., Watanabe T., Lin C.S., William C.M., Tanabe Y., Jessell T.M., Costantini F. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 2001, 1:4.
59. Tischfield M.A., Bosley T.M., Salih M.A., Alorainy I.A., Sener E.C., Nester M.J., Oystreck D.T., Chan W.M., Andrews C., Erickson R.P., Engle E.C. Homozygous HOXA1 mutations disrupt human brainstem, inner ear, cardiovascular and cognitive development. Nat. Genet. 2005, 37:1035-1037.
60. Torres M., Giraldez F. The development of the vertebrate inner ear. Mech. Dev. 1998, 71:5-21.
61. Wang M., Drucker D.J. The LIM domain homeobox gene isl-1: conservation of human, hamster, and rat complementary deoxyribonucleic acid sequences and expression in cell types of nonneuroendocrine lineage. Endocrinology 1994, 134:1416-1422.
62. Wassef M.A., Chomette D., Pouilhe M., Stedman A., Havis E., Desmarquet-Trin Dinh C., Schneider-Maunoury S., Gilardi-Hebenstreit P., Charnay P., Ghislain J. Rostral hindbrain patterning involves the direct activation of a Krox20 transcriptional enhancer by Hox/Pbx and Meis factors. Development 2008, 135:3369-3378.
63. Wright W.E., Sassoon D.A., Lin V.K. Myogenin, a factor regulating myogenesis, has a domain homologous to MyoD. Cell 1989, 56:607-617.
64. Zhao Q., Eberspaecher H., Lefebvre V., De Crombrugghe B. Parallel expression of Sox9 and Col2a1 in cells undergoing chondrogenesis. Dev. Dyn. 1997, 209:377-386.