Role of pax genes in eye evolution: A Cnidarian PaxB gene uniting Pax2 and Pax6 functions

Developmental Cell

Volumn 5, Issue 5, 2003, Pages 773-785

  Kozmik, Zbynek ^a,d   Daube, Michael ^b   Frei, Erich ^a   Norman, Barbara ^a   Kos, Lidia ^c   Dishaw, Larry J ^c   Noll, Markus ^b   Piatigorsky, Joram ^a  

^a NATIONAL EYE INSTITUTE   (United States)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c FLORIDA INTERNATIONAL UNIVERSITY   (United States)

^d INSTITUTE OF MOLECULAR GENETICS   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

CRYSTALLIN; DROSOPHILA PROTEIN; HOMEODOMAIN PROTEIN; MUTANT PROTEIN; OCTAPEPTIDE; PROTEIN PRECURSOR; RHODOPSIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PAX2; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR PAXB; UNCLASSIFIED DRUG;

ARTICLE; COELENTERATE; CONTROLLED STUDY; DNA BINDING; EYE DEVELOPMENT; EYE MALFORMATION; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION; LARVA; LENS; NONHUMAN; NUCLEOTIDE SEQUENCE; OTOLITH; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; RETINA; SEPARATION TECHNIQUE;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BINDING SITES; CNIDARIA; CRYSTALLINS; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EVOLUTION; EYE; EYE PROTEINS; GENES, REPORTER; HOMEODOMAIN PROTEINS; MOLECULAR SEQUENCE DATA; OCULAR PHYSIOLOGY; PAIRED BOX TRANSCRIPTION FACTORS; PAX2 TRANSCRIPTION FACTOR; PHENOTYPE; PHOTORECEPTORS, INVERTEBRATE; PROMOTER REGIONS (GENETICS); PROTEINS; RECOMBINANT FUSION PROTEINS; REPRESSOR PROTEINS; RHODOPSIN; SEQUENCE ALIGNMENT; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTORS;

CNIDARIA; COELENTERATA; INVERTEBRATA; SCYPHOZOA; TRIPEDALIA CYSTOPHORA;

EID: 0242268030     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1534-5807(03)00325-3     Document Type: Article

References (72)

1. Adams B. Dörfler P. Aguzzi A. Kozmik Z. Urbánek P. Maurer-Fogy I. Busslinger M. Pax-5 encodes the transcription factor BSAP and is expressed in B lymphocytes, the developing CNS, and adult testis Genes Dev. 6 1992 1589-1607
2. Arendt D. Tessmar K. Medeiros de Campos-Baptista M.-I. Dorresteijn A. Wittbrodt J. Development of pigment-cup eyes in the polychaete Platynereis dumerilii and evolutionary conservation of larval eyes in Bilateria Development 129 2002 1143-1154
3. Balczarek K.A. Lai Z.-C. Kumar S. Evolution and functional diversification of the paired box (Pax) DNA-binding domains Mol. Biol. Evol. 14 1997 829-842
4. Barberis A. Superti-Furga G. Vitelli L. Kemler I. Busslinger M. Developmental and tissue-specific regulation of a novel transcription factor of the sea urchin Genes Dev. 3 1989 663-675
5. Bopp D. Burri M. Baumgartner S. Frigerio G. Noll M. Conservation of a large protein domain in the segmentation gene paired and in functionally related genes of Drosophila Cell 47 1986 1033-1040
6. Bouchard M. Souabni A. Mandler M. Neubüser A. Busslinger M. Nephric lineage specification by Pax2 and Pax8 Genes Dev. 16 2002 2958-2970
7. Carosa E. Kozmik Z. Rall J.E. Piatigorsky J. Structure and expression of the scallop Ω-crystallin gene. Evidence for convergent evolution of promoter sequences J. Biol. Chem. 277 2002 656-664
8. Chen R. Amoui M. Zhang Z. Mardon G. Dachshund and Eyes Absent proteins form a complex and function synergistically to induce ectopic eye development in Drosophila Cell 91 1997 893-903
9. Chi N. Epstein J.A. Getting your Pax straight: Pax proteins in development and disease Trends Genet. 18 2002 41-47
10. Collins A.G. Phylogeny of Medusozoa and the evolution of cnidarian life cycles J. Evol. Biol. 15 2002 418-432
11. Cvekl A. Piatigorsky J. Lens development and crystallin gene expression: many roles for Pax-6 BioEssays 18 1996 621-630
12. Czerny T. Busslinger M. DNA-binding and transactivation properties of Pax-6: three amino acids in the paired domain are responsible for the different sequence recognition of Pax-6 and BSAP (Pax-5) Mol. Cell. Biol. 15 1995 2858-2871
13. Czerny T. Schaffner G. Busslinger M. DNA sequence recognition by Pax proteins: bipartite structure of the paired domain and its binding site Genes Dev. 7 1993 2048-2061
14. Czerny T. Bouchard M. Kozmik Z. Busslinger M. The characterization of novel Pax genes of the sea urchin and Drosophila reveal an ancient evolutionary origin of the Pax2/5/8 subfamily Mech. Dev. 67 1997 179-192
15. Czerny T. Halder G. Kloter U. Souabni A. Gehring W.J. Busslinger M. twin of eyeless, a second Pax-6 gene of Drosophila, acts upstream of eyeless in the control of eye development Mol. Cell 3 1999 297-307
16. Davis J.A. Reed R.R. Role of Olf-1 and Pax-6 transcription factors in neurodevelopment J. Neurosci. 16 1996 5082-5094
17. de Jong W.W. Hendriks W. Mulders J.W.M. Bloemendal H. Evolution of eye lens crystallins: the stress connection Trends Biochem. Sci. 14 1989 365-368
18. Dörfler P. Busslinger M. C-terminal activating and inhibitory domains determine the transactivation potential of BSAP (Pax-5), Pax-2 and Pax-8 EMBO J. 15 1996 1971-1982
19. Duncan, M.K., Cvekl, A., Kantorow, M., and Piatigorsky, J. (2004). Lens crystallins. In Development of the Ocular Lens, F.J. Lovicu and M.L. Robinson, eds. (Cambridge: Cambridge University Press), in press.
20. Eakin R.M. Evolutionary significance of photoreceptors: in retrospect Am. Zool. 19 1979 647-653
21. Eberhard D. Jiménez G. Heavey B. Busslinger M. Transcriptional repression by Pax5 (BSAP) through interaction with corepressors of the Groucho family EMBO J. 19 2000 2292-2303
22. Flores G.V. Duan H. Yan H. Nagaraj R. Fu W. Zou Y. Noll M. Banerjee U. Combinatorial signaling in the specification of unique cell fates Cell 103 2000 75-85
23. Fu W. Noll M. The Pax2 homolog sparkling is required for development of cone and pigment cells in the Drosophila eye Genes Dev. 11 1997 2066-2078
24. Fu W. Duan H. Frei E. Noll M. shaven and sparkling are mutations in separate enhancers of the Drosophila Pax2 homolog Development 125 1998 2943-2950
25. Galliot B. Schmid V. Cnidarians as a model system for understanding evolution and regeneration Int. J. Dev. Biol. 46 2002 39-48
26. Gehring W.J. The genetic control of eye development and its implications for the evolution of the various eye-types Int. J. Dev. Biol. 46 2002 65-73
27. Gehring W.J. Ikeo K. Pax 6: mastering eye morphogenesis and eye evolution Trends Genet. 15 1999 371-377
28. Gröger H. Callaerts P. Gehring W.J. Schmid V. Characterization and expression analysis of an ancestor-type Pax gene in the hydrozoan jellyfish Podocoryne carnea Mech. Dev. 94 2000 157-169
29. Halder G. Callaerts P. Gehring W.J. Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila Science 267 1995 1788-1792
30. Hanson I. van Heyningen V. Pax6: more than meets the eye Trends Genet. 11 1995 268-272
31. Hill M.E. Asa S.L. Drucker D.J. Essential requirement for Pax6 in control of enteroendocrine proglucagon gene transcription Mol. Endocrinol. 13 1999 1474-1486
32. Hoshiyama D. Suga H. Iwabe N. Koyanagi M. Nikoh N. Kuma K. Matsuda F. Honjo T. Miyata T. Sponge Pax cDNA related to Pax-2/5/8 and ancient gene duplications in the Pax family J. Mol. Evol. 47 1998 640-648
33. Kamachi Y. Uchikawa M. Tanouchi A. Sekido R. Kondoh H. Pax6 and SOX2 form a co-DNA-binding partner complex that regulates initiation of lens development Genes Dev. 15 2001 1272-1286
34. Kavaler J. Fu W. Duan H. Noll M. Posakony J.W. An essential role for the Drosophila Pax2 homolog in the differentiation of adult sensory organs Development 126 1999 2261-2272
35. Kostrouch Z. Kostrouchova M. Love W. Jannini E. Piatigorsky J. Rall J.E. Retinoic acid X receptor in the diploblast, Tripedalia cystophora Proc. Natl. Acad. Sci. USA 95 1998 13442-13447
36. Kozmik Z. Wang S. Dörfler P. Adams B. Busslinger M. The promoter of the CD19 gene is a target for the B-cell-specific transcription factor BSAP Mol. Cell. Biol. 12 1992 2662-2672
37. Kreslová J. Holland L.Z. Schubert M. Burgtorf C. Benes V. Kozmik Z. Functional equivalency of amphioxus and vertebrate Pax258 transcription factors suggests that the activation of mid-hindbrain specific genes in vertebrates occurs via the recruitment of Pax regulatory elements Gene 282 2002 143-150
38. Land M.F. Nilsson D.-E. Animal Eyes 2002 Oxford University Press Oxford
39. Lechner M.S. Dressler G.R. Mapping of Pax-2 transcription activation domains J. Biol. Chem. 271 1996 21088-21093
40. Mansouri A. Chowdhury K. Gruss P. Follicular cells of the thyroid gland require Pax8 gene function Nat. Genet. 19 1998 87-90
41. Miller D.J. Hayward D.C. Reece-Hoyes J.S. Scholten I. Catmull J. Gehring W.J. Callaerts P. Larsen J.E. Ball E.E. Pax gene diversity in the basal cnidarian Acropora millepora (Cnidaria, Anthozoa): implications for the evolution of the Pax gene family Proc. Natl. Acad. Sci. USA 97 2000 4475-4480
42. Nilsson D.-E. Pelger S. A pessimistic estimate of the time required for an eye to evolve Proc. R. Soc. Lond. B. Biol. Sci. 256 1994 53-58
43. Noll M. Evolution and role of Pax genes Curr. Opin. Genet. Dev. 3 1993 595-605
44. Nornes S. Clarkson M. Mikkola I. Pedersen M. Bardsley A. Martinez J.P. Krauss S. Johansen T. Zebrafish contains two Pax6 genes involved in eye development Mech. Dev. 77 1998 185-196
45. Nutt S.L. Heavey B. Rolink A.G. Busslinger M. Commitment to the B-lymphoid lineage depends on the transcription factor Pax5 Nature 401 1999 556-562
46. Papatsenko D. Nazina A. Desplan C. A conserved regulatory element present in all Drosophila rhodopsin genes mediates Pax6 functions and participates in the fine-tuning of cell-specific expression Mech. Dev. 101 2001 143-153
47. Pfeffer P.L. Gerster T. Lun K. Brand M. Busslinger M. Characterization of three novel members of the zebrafish Pax2/5/8 family: dependency of Pax5 and Pax8 expression on the Pax2.1 (noi) function Development 125 1998 3063-3074
48. Piatigorsky J. Horwitz J. Kuwabara T. Cutress C.E. The cellular eye lens and crystallins of cubomedusan jellyfish J. Comp. Physiol. [A] 164 1989 577-587
49. Piatigorsky J. Horwitz J. Norman B.L. J1-crystallins of the cubomedusan jellyfish lens constitute a novel family encoded in at least three intronless genes J. Biol. Chem. 268 1993 11894-11901
50. Piatigorsky J. Norman B. Dishaw L.J. Kos L. Horwitz J. Steinbach P.J. Kozmik Z. J3-crystallin of the jellyfish lens: similarity to saposins Proc. Natl. Acad. Sci. USA 98 2001 12362-12367
51. Pignoni F. Hu B. Zavitz K.H. Xiao J. Garrity P.A. Zipursky S.L. The eye-specification proteins So and Eya form a complex and regulate multiple steps in Drosophila eye development Cell 91 1997 881-891
52. Pineda D. Rossi L. Batistoni R. Salvetti A. Marsal M. Gremigni V. Falleni A. Gonzalez-Linares J. Deri P. Saló E. The genetic network of prototypic planarian eye regeneration is Pax6 independent Development 129 2002 1423-1434
53. Punzo C. Kurata S. Gehring W.J. The eyeless homeodomain is dispensable for eye development in Drosophila Genes Dev. 15 2001 1716-1723
54. Quiring R. Walldorf U. Kloter U. Gehring W.J. Homology of the eyeless gene of Drosophila to the Small eye gene in mice and Aniridia in humans Science 265 1994 785-789
55. Rolink A.G. Nutt S.L. Melchers F. Busslinger M. Long-term in vivo reconstitution of T-cell development by Pax5-deficient B-cell progenitors Nature 401 1999 603-606
56. Schreiber E. Matthias P. Müller M.M. Schaffner W. Rapid detection of octamer binding proteins with 'mini-extracts,' prepared from a small number of cells Nucleic Acids Res. 17 1989 6419
57. Schwarz M. Alvarez-Bolado G. Urbánek P. Busslinger M. Gruss P. Conserved biological function between Pax-2 and Pax-5 in midbrain and cerebellum development: evidence from targeted mutations Proc. Natl. Acad. Sci. USA 94 1997 14518-14523
58. Sheng G. Thouvenot E. Schmucker D. Wilson D.S. Desplan C. Direct regulation of rhodopsin 1 by Pax-6/eyeless in Drosophila: evidence for a conserved function in photoreceptors Genes Dev. 11 1997 1122-1131
59. Stifani S. Blaumueller C.M. Redhead N.J. Hill R.E. Artavanis-Tsakonas S. Human homologs of a Drosophila Enhancer of Split gene product define a novel family of nuclear proteins Nat. Genet. 2 1992 119-127
60. Sun H. Rodin A. Zhou Y. Dickinson D.P. Harper D.E. Hewett-Emmett D. Li W.-H. Evolution of paired domains: isolation and sequencing of jellyfish and hydra Pax genes related to Pax-5 and Pax-6 Proc. Natl. Acad. Sci. USA 94 1997 5156-5161
61. Sun H. Dickinson D.P. Costello J. Li W.-H. Isolation of Cladonema Pax-B genes and studies of the DNA-binding properties of cnidarian Pax paired domains Mol. Biol. Evol. 18 2001 1905-1918
62. Tang H.K. Singh S. Saunders G.F. Dissection of the transactivation function of the transcription factor encoded by the eye developmental gene PAX6 J. Biol. Chem. 273 1998 7210-7221
63. Tomarev S.I. Piatigorsky J. Lens crystallins of invertebrates. Diversity and recruitment from detoxification enzymes and novel proteins Eur. J. Biochem. 235 1996 449-465
64. Torres M. Gómez-Pardo E. Gruss P. Pax2 contributes to inner ear patterning and optic nerve trajectory Development 122 1996 3381-3391
65. Treisman J. Harris E. Desplan C. The paired box encodes a second DNA-binding domain in the paired homeo domain protein Genes Dev. 5 1991 594-604
66. Urbánek P. Wang Z.-Q. Fetka I. Wagner E.F. Busslinger M. Complete block of early B cell differentiation and altered patterning of the posterior midbrain in mice lacking Pax5/BSAP Cell 79 1994 901-912
67. Urbánek P. Fetka I. Meisler M.H. Busslinger M. Cooperation of Pax2 and Pax5 in midbrain and cerebellum development Proc. Natl. Acad. Sci. USA 94 1997 5703-5708
68. Wilkinson D.G. Nieto M.A. Detection of messenger RNA by in situ hybridization to tissue sections and whole mounts Methods Enzymol. 225 1993 361-373
69. Wistow G.J. Piatigorsky J. Lens crystallins: the evolution and expression of proteins for a highly specialized tissue Annu. Rev. Biochem. 57 1988 479-504
70. Xu W. Rould M.A. Jun S. Desplan C. Pabo C.O. Crystal structure of a paired domain-DNA complex at 2.5 Å resolution reveals structural basis for Pax developmental mutations Cell 80 1995 639-650
71. Xu H.E. Rould M.A. Xu W. Epstein J.A. Maas R.L. Pabo C.O. Crystal structure of the human Pax6 paired domain-DNA complex reveals specific roles for the linker region and carboxy-terminal subdomain in DNA binding Genes Dev. 13 1999 1263-1275
72. Zannini M. Francis-Lang H. Plachov D. Di Lauro R. Pax-8, a paired domain-containing protein, binds to a sequence overlapping the recognition site of a homeodomain and activates transcription from two thyroid-specific promoters Mol. Cell. Biol. 12 1992 4230-4241