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March 18, 1992, Vol 267, No. 11 >
ARTICLE | March 18, 1992

Clusters of Master Control Genes Regulate the Development of Higher Organisms FREE

Edward B. Lewis, PhD
[+] Author Affiliations

The 1991 Albert Lasker Medical Award was presented to Dr Lewis on September 27,1991,in New York City.

Reprint requests to Division of Biology, California Institute of Technology, Pasadena, CA 91125 (Dr Lewis).


JAMA. 1992;267(11):1524-1531. doi:10.1001/jama.1992.03480110100042
Text Size: A A A
Published online
Article
References

REFERENCES

1 +
Sturtevant AH.  The effects of unequal crossing over at the Bar locus in Drosophila. Genetics . 1925;;10:117-147.
2 +
Maeda N, Smithies O.  The evolution of multigene families: human haptoglobin genes. Annu Rev Genet . 1986;;20:81-108.
3 +
Bridges CB.  The Bar 'gene': a duplication. Science . 1936;;83:210-211.
4 +
Muller HJ, Prokofyeva-Belgovskaya AA, Kossikov KV.  Unequal crossing-over in the Bar mutant as a result of duplication of a minute chromosome section. Comptes Rendus (Doklady) el l'Académie des Sciences del l'URSS . 1936;;I:87-88.
5 +
Rapoport JA.  Quadruple-Bar in Drosophila melanogaster. Bull Biol Med Exp . 1936;;II:242-244.
6 +
Lindsley DL, Grell EH. Genetic Variations of Drosophila melanogaster . Washington, DC: Carnegie Institution of Washington; 1968;:1-521. Publication 627.
7 +
Bridges CB.  Salivary chromosome maps with a key to the banding of the chromosomes of Drosophila melanogaster. J Hered . 1935;;26:60-64.
8 +
Oliver CP.  A reversion to wild-type associated with crossing over in Drosophila melanogaster. Proc Natl Acad Sci U S A . 1940;;26:452-454.
9 +
Lewis EB.  Star-recessive, a spontaneous mutation in Drosophila melanogaster. Proc Minn Acad Sci . 1939;;7:23-26.
10 +
Lewis EB.  The Star and asteroid loci in Drosophila melanogaster. Genetics . 1942;;27:153-154.
11 +
Lewis EB.  Pseudoallelism and gene evolution. Cold Spring Harbor Symp Quant Biol . 1951;;16:159-174.
12 +
Green MM, Green KC.  Crossing-over between alleles at the lozenge locus in Drosophila melanogaster. Proc Natl Acad Sci U S A . 1949;;35:586-591.
13 +
Hayes W. The Genetics of Bacteria and Their Viruses: Studies in Basic Genetics and Molecular Biology . 2nd ed. New York, NY: John Wiley & Sons Inc; 1968;.
14 +
Lewis EB.  The relation repeats to position effect in Drosophila melanogaster. Genetics . 1945;;30:137-166.
15 +
Lewis EB.  A gene complex controlling segmentation in Drosophila. Nature . 1978;;276:565-570.
16 +
Jacob F, Monod J.  On the regulation of gene activity. Cold Spring Harbor Symp . 1961;;26:193-211.
17 +
Lewis EB.  Genetic control and regulation of developmental pathways.  In: Locke M, ed. Role of Chromosomes in Development . New York, NY: Academic Press Inc; 1964;:231-252.
18 +
Duncan I.  The bithorax complex. Annu Rev Genet . 1987;;21:285-319.
19 +
Lewis EB.  Regulation of the genes of the bithorax complex in Drosophila. Cold Spring Harbor Symp Quant Biol . 1986;;50:155-164.
20 +
Bender W, Akam M, Karch F, et al.  Molecular genetics of the bithorax complex in Drosophila melanogaster. Science . 1983;;221:23-29.
21 +
Karch F, Weiffenbach B, Peifer M, et al.  The abdominal region of the bithorax complex. Cell . 1985;;43:81-96.
22 +
Celniker SE, Lewis EB.  Transabdominal: a dominant mutant of the bithorax complex produces a sexually dimorphic segmental transformation in Drosophila. Gene Dev . 1987;;1:111-123.
23 +
Kornfeld K, Saint RB, Beachy PA, Harte PJ, Peattie DA, Hogness DS.  Structure and expression of a family of Ultrabithorax mRNAs generated by alternative splicing and polyadenylation in Drosophila. Genes Dev . 1989;;3:243-258.
24 +
White RAH, Wilcox M.  Protein products of the bithorax complex in Drosophila. Cell . 1984;;39:163-171.
25 +
Beachy PA, Helfand SL, Hogness DS.  Segmental distribution of bithorax complex proteins during Drosophila development. Nature . 1985;; 313:545-551.
26 +
Lawrence PA, Martinez-Arias A.  The cell lineage of segments and parasegments in Drosophila. Philos Trans R Soc Lond Biol . 1985;;312:83-90.
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Hogness DS, Lipshitz H, Beachy DA, et al.  Regulation and products of the Ubx domain of the bithorax complex. Cold Spring Harbor Symp Quant Biol . 1985;;50:181-194.
28 +
Karch F, Bender W, Weiffenbach B.  abdA expression in Drosophila embryos. Genes Dev . 1990;;4:1573-1587.
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Macias A, Casanova J, Morata G.  Expression and regulation of the abd-A gene of Drosophila. Development . 1990;;110:1197-1207.
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Celniker SE, Keelan DJ, Lewis EB.  The molecular genetics of the bithorax complex of Drosophila: characterization of the products of the Abdominal-B domain. Genes Dev . 1989;;3:1424-1436.
31 +
Delorenzi M, Bienz M.  Expression of Abdominal-B homeoproteins in Drosophila embryos. Development . 1990;;108:323-329.
32 +
Boulet AM, Lloyd A, Sakonju S.  Molecular definition of the morphogenetic and regulatory functions and the cis-regulatory elements of the Drosophila Abd-B homeotic gene. Development . 1991;; 111:393-405.
33 +
Celniker SE, Sharma S, Keelan DJ, Lewis EB.  The molecular genetics of the bithorax complex of Drosophila: cis-regulation in the Abdominal-B domain. EMBO J . 1990;;9:4277-4286.
34 +
Sanchez-Herrero E, Akam M.  Spatially ordered transcription of regulatory DNA in the bithorax complex of Drosophila. Development . 1989;;107:321-329.
35 +
Lipshitz H, Peattie D, Hogness D.  Novel transcripts from the Ultrabithorax domain of the bithorax complex. Genes Dev . 1987;;1:307-322.
36 +
Kaufman TC, Seeger MA, Olsen G.  Molecular and genetic organization of the Antennapedia gene complex of Drosophila melanogaster. Adv Genet . 1990;;27:309-362.
37 +
Sturtevant AH.  Genetic data on Drosophila affinis, with a discussion of the relationships in the subgenus Sophophora. Genetics . 1940;;25:337-353.
38 +
Kaufman TC, Lewis R, Wakimoto B.  Cytogenetic analysis of chromosome 3 in Drosophila melanogaster: the homeotic gene complex in polytene chromosomal interval 84A,B. Genetics . 1980;;94:115-133.
39 +
Garber RL, Kuroiwa A, Gehring WJ.  Genomic and cDNA clones of the homeotic locus Antennapedia in Drosophila. EMBO J . 1983;;2:2027-2036.
40 +
Scott MP, Weiner AJ, Hazelrigg TI, et al.  The molecular organization of the Antennapedia locus of Drosophila. Cell . 1983;;35:763-776.
41 +
Nüsslein-Volhard C, Wieschaus E.  Mutations affecting segment number and polarity in Drosophila. Nature . 1980;;287:795-801.
42 +
Nüsslein-Volhard C, Frohnhofer HG, Lehmann R.  Determination of anteroposterior polarity in Drosophila. Science . 1987;;230:1675-1681.
43 +
Ingham PW.  The molecular genetics of embryonic pattern formation in Drosophila. Nature . 1988;;335:25-34.
44 +
Lewis EB. Genetic control of developmental pathways in Drosophila melanogaster. Presented at the XII International Congress on Genetics; August 26, 1968:96-97; Tokyo, Japan.
45 +
Bender M, Turner FR, Kaufman TC.  A developmental genetic analysis of the gene regulator of postbithorax in Drosophila melanogaster. Dev Biol . 1987;;119:418-432.
46 +
Garcia-Bellido A, Capdevila MP.  The initiation and maintenance of gene activity in a developmental pathway of Drosophila.  In: Subtelny S, Sussex IM, eds. The Clonal Basis of Development: 36th Symposium of the Society for Developmental Biology . Orlando, Fla: Academic Press Inc; 1978;:3-21.
47 +
Qian S, Capovilla M, Pirrotta V.  The bx region enhancer, a distant cis-control element of the Drosophila Ubx gene and its regulation by hunchback and other segmentation genes. EMBO J . 1991;;10:1415-1425.
48 +
Ingham PW, Martinez-Arias A.  The correct activation of Antennapedia and bithorax complex genes requires the fushi-tarazu gene. Nature . 1986;;324:592-597.
49 +
Ingham PW, Ish-Horowicz D, Howard KR.  Correlative changes in homeotic and segmentation gene expression in Krüppel mutant embryos in Drosophila. EMBO J . 1986;;5:1659-1665.
50 +
Martinez-Arias A, White RAH.  Ultrabithorax and engrailed expression in Drosophila embryos mutant for segmentation genes of the pair-rule class. Development . 1988;;102:325-338.
51 +
Irish VF, Martinez-Arias A, Akam M.  Spatial regulation of the Antennapedia-homeotic and Ultrabithorax-homeotic genes during Drosophila early development. EMBO J . 1989;;8:1527-1537.
52 +
Zink B, Paro R.  In vivo binding pattern of a trans-regulator of homeotic genes in Drosophila melanogaster. Nature . 1989;;337:468-471.
53 +
Zink B, Engstrom Y, Gehring WJ, Paro R.  Direct interaction of the polycomb protein with Antennapedia regulatory sequences in polytene chromosomes of Drosophila melanogaster. EMBO J . 1991;;10:153-162.
54 +
Paro R, Hogness DS.  The Polycomb protein shares a homologous domain with a heterochromatin-associated protein of Drosophila. Proc Natl Acad Sci U S A . 1991;;88:263-267.
55 +
Struhl G.  Genes controlling segmental specification in the Drosophila thorax. Proc Natl Acad Sci U S A . 1982;;79:7380-7384.
56 +
Struhl G, Akam M.  Altered distributions of Ultrabithorax transcripts in extra sex combs mutant embryos of Drosophila. EMBO J . 1985;;4:3259-3264.
57 +
Ingham PW, Whittle JRS.  Trithorax: a new homeotic mutation of Drosophila melanogaster causing transformations of abdominal and thoracic imaginal segments. J Mol Gen Genet . 1980;;179:607.
58 +
Ingham PW.  A new homeotic mutation of Drosophila melanogaster, II: the role of trx+ after embryogenesis. Wilhelm Rouxs Arch Dev Biol . 1981;;190:365.
59 +
McGinnis W, Levine M, Hafen E, Kuroiwa A, Gehring WJ.  A conserved DNA sequence found in homeotic genes of the Drosophila Antennapediaand bithorax complexes. Nature . 1984;;308:428-433.
60 +
Scott MP, Weiner AJ.  Structural relationships among genes that control development: sequence homology between the Antennapedia, Ultrabithorax, and fushi tarazu loci of Drosophila. Proc Natl Acad Sci U S A . 1984;;81:4115-4119.
61 +
Beeman RW.  A homeotic gene cluster in the red flour beetle. Nature . 1987;;327:247-249.
62 +
Beeman RW, Stuart JJ, Haas MS, Dennell RE.  Genetic analysis of the homeotic gene complex (HOM-C) in the beetle Tribolium castaneum. Dev Biol . 1989;;133:196-209.
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Tsujita M.  On the crossing-over between EH and EK of the E allelic series in the silkworm. Jpn J Genet . 1955;;30:227-235.
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Bender W, Weiffenbach B, Karch F, Peifer M.  Domains of cis-interaction in the bithorax complex. Cold Spring Harbor Symp Quant Biol . 1985;;I:173-180.
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Country-Specific Mortality and Growth Failure in Infancy and Yound Children and Association With Material Stature

Use interactive graphics and maps to view and sort country-specific infant and early dhildhood mortality and growth failure data and their association with maternal

1 +
Sturtevant AH.  The effects of unequal crossing over at the Bar locus in Drosophila. Genetics . 1925;;10:117-147.
2 +
Maeda N, Smithies O.  The evolution of multigene families: human haptoglobin genes. Annu Rev Genet . 1986;;20:81-108.
3 +
Bridges CB.  The Bar 'gene': a duplication. Science . 1936;;83:210-211.
4 +
Muller HJ, Prokofyeva-Belgovskaya AA, Kossikov KV.  Unequal crossing-over in the Bar mutant as a result of duplication of a minute chromosome section. Comptes Rendus (Doklady) el l'Académie des Sciences del l'URSS . 1936;;I:87-88.
5 +
Rapoport JA.  Quadruple-Bar in Drosophila melanogaster. Bull Biol Med Exp . 1936;;II:242-244.
6 +
Lindsley DL, Grell EH. Genetic Variations of Drosophila melanogaster . Washington, DC: Carnegie Institution of Washington; 1968;:1-521. Publication 627.
7 +
Bridges CB.  Salivary chromosome maps with a key to the banding of the chromosomes of Drosophila melanogaster. J Hered . 1935;;26:60-64.
8 +
Oliver CP.  A reversion to wild-type associated with crossing over in Drosophila melanogaster. Proc Natl Acad Sci U S A . 1940;;26:452-454.
9 +
Lewis EB.  Star-recessive, a spontaneous mutation in Drosophila melanogaster. Proc Minn Acad Sci . 1939;;7:23-26.
10 +
Lewis EB.  The Star and asteroid loci in Drosophila melanogaster. Genetics . 1942;;27:153-154.
11 +
Lewis EB.  Pseudoallelism and gene evolution. Cold Spring Harbor Symp Quant Biol . 1951;;16:159-174.
12 +
Green MM, Green KC.  Crossing-over between alleles at the lozenge locus in Drosophila melanogaster. Proc Natl Acad Sci U S A . 1949;;35:586-591.
13 +
Hayes W. The Genetics of Bacteria and Their Viruses: Studies in Basic Genetics and Molecular Biology . 2nd ed. New York, NY: John Wiley & Sons Inc; 1968;.
14 +
Lewis EB.  The relation repeats to position effect in Drosophila melanogaster. Genetics . 1945;;30:137-166.
15 +
Lewis EB.  A gene complex controlling segmentation in Drosophila. Nature . 1978;;276:565-570.
16 +
Jacob F, Monod J.  On the regulation of gene activity. Cold Spring Harbor Symp . 1961;;26:193-211.
17 +
Lewis EB.  Genetic control and regulation of developmental pathways.  In: Locke M, ed. Role of Chromosomes in Development . New York, NY: Academic Press Inc; 1964;:231-252.
18 +
Duncan I.  The bithorax complex. Annu Rev Genet . 1987;;21:285-319.
19 +
Lewis EB.  Regulation of the genes of the bithorax complex in Drosophila. Cold Spring Harbor Symp Quant Biol . 1986;;50:155-164.
20 +
Bender W, Akam M, Karch F, et al.  Molecular genetics of the bithorax complex in Drosophila melanogaster. Science . 1983;;221:23-29.
21 +
Karch F, Weiffenbach B, Peifer M, et al.  The abdominal region of the bithorax complex. Cell . 1985;;43:81-96.
22 +
Celniker SE, Lewis EB.  Transabdominal: a dominant mutant of the bithorax complex produces a sexually dimorphic segmental transformation in Drosophila. Gene Dev . 1987;;1:111-123.
23 +
Kornfeld K, Saint RB, Beachy PA, Harte PJ, Peattie DA, Hogness DS.  Structure and expression of a family of Ultrabithorax mRNAs generated by alternative splicing and polyadenylation in Drosophila. Genes Dev . 1989;;3:243-258.
24 +
White RAH, Wilcox M.  Protein products of the bithorax complex in Drosophila. Cell . 1984;;39:163-171.
25 +
Beachy PA, Helfand SL, Hogness DS.  Segmental distribution of bithorax complex proteins during Drosophila development. Nature . 1985;; 313:545-551.
26 +
Lawrence PA, Martinez-Arias A.  The cell lineage of segments and parasegments in Drosophila. Philos Trans R Soc Lond Biol . 1985;;312:83-90.
27 +
Hogness DS, Lipshitz H, Beachy DA, et al.  Regulation and products of the Ubx domain of the bithorax complex. Cold Spring Harbor Symp Quant Biol . 1985;;50:181-194.
28 +
Karch F, Bender W, Weiffenbach B.  abdA expression in Drosophila embryos. Genes Dev . 1990;;4:1573-1587.
29 +
Macias A, Casanova J, Morata G.  Expression and regulation of the abd-A gene of Drosophila. Development . 1990;;110:1197-1207.
30 +
Celniker SE, Keelan DJ, Lewis EB.  The molecular genetics of the bithorax complex of Drosophila: characterization of the products of the Abdominal-B domain. Genes Dev . 1989;;3:1424-1436.
31 +
Delorenzi M, Bienz M.  Expression of Abdominal-B homeoproteins in Drosophila embryos. Development . 1990;;108:323-329.
32 +
Boulet AM, Lloyd A, Sakonju S.  Molecular definition of the morphogenetic and regulatory functions and the cis-regulatory elements of the Drosophila Abd-B homeotic gene. Development . 1991;; 111:393-405.
33 +
Celniker SE, Sharma S, Keelan DJ, Lewis EB.  The molecular genetics of the bithorax complex of Drosophila: cis-regulation in the Abdominal-B domain. EMBO J . 1990;;9:4277-4286.
34 +
Sanchez-Herrero E, Akam M.  Spatially ordered transcription of regulatory DNA in the bithorax complex of Drosophila. Development . 1989;;107:321-329.
35 +
Lipshitz H, Peattie D, Hogness D.  Novel transcripts from the Ultrabithorax domain of the bithorax complex. Genes Dev . 1987;;1:307-322.
36 +
Kaufman TC, Seeger MA, Olsen G.  Molecular and genetic organization of the Antennapedia gene complex of Drosophila melanogaster. Adv Genet . 1990;;27:309-362.
37 +
Sturtevant AH.  Genetic data on Drosophila affinis, with a discussion of the relationships in the subgenus Sophophora. Genetics . 1940;;25:337-353.
38 +
Kaufman TC, Lewis R, Wakimoto B.  Cytogenetic analysis of chromosome 3 in Drosophila melanogaster: the homeotic gene complex in polytene chromosomal interval 84A,B. Genetics . 1980;;94:115-133.
39 +
Garber RL, Kuroiwa A, Gehring WJ.  Genomic and cDNA clones of the homeotic locus Antennapedia in Drosophila. EMBO J . 1983;;2:2027-2036.
40 +
Scott MP, Weiner AJ, Hazelrigg TI, et al.  The molecular organization of the Antennapedia locus of Drosophila. Cell . 1983;;35:763-776.
41 +
Nüsslein-Volhard C, Wieschaus E.  Mutations affecting segment number and polarity in Drosophila. Nature . 1980;;287:795-801.
42 +
Nüsslein-Volhard C, Frohnhofer HG, Lehmann R.  Determination of anteroposterior polarity in Drosophila. Science . 1987;;230:1675-1681.
43 +
Ingham PW.  The molecular genetics of embryonic pattern formation in Drosophila. Nature . 1988;;335:25-34.
44 +
Lewis EB. Genetic control of developmental pathways in Drosophila melanogaster. Presented at the XII International Congress on Genetics; August 26, 1968:96-97; Tokyo, Japan.
45 +
Bender M, Turner FR, Kaufman TC.  A developmental genetic analysis of the gene regulator of postbithorax in Drosophila melanogaster. Dev Biol . 1987;;119:418-432.
46 +
Garcia-Bellido A, Capdevila MP.  The initiation and maintenance of gene activity in a developmental pathway of Drosophila.  In: Subtelny S, Sussex IM, eds. The Clonal Basis of Development: 36th Symposium of the Society for Developmental Biology . Orlando, Fla: Academic Press Inc; 1978;:3-21.
47 +
Qian S, Capovilla M, Pirrotta V.  The bx region enhancer, a distant cis-control element of the Drosophila Ubx gene and its regulation by hunchback and other segmentation genes. EMBO J . 1991;;10:1415-1425.
48 +
Ingham PW, Martinez-Arias A.  The correct activation of Antennapedia and bithorax complex genes requires the fushi-tarazu gene. Nature . 1986;;324:592-597.
49 +
Ingham PW, Ish-Horowicz D, Howard KR.  Correlative changes in homeotic and segmentation gene expression in Krüppel mutant embryos in Drosophila. EMBO J . 1986;;5:1659-1665.
50 +
Martinez-Arias A, White RAH.  Ultrabithorax and engrailed expression in Drosophila embryos mutant for segmentation genes of the pair-rule class. Development . 1988;;102:325-338.
51 +
Irish VF, Martinez-Arias A, Akam M.  Spatial regulation of the Antennapedia-homeotic and Ultrabithorax-homeotic genes during Drosophila early development. EMBO J . 1989;;8:1527-1537.
52 +
Zink B, Paro R.  In vivo binding pattern of a trans-regulator of homeotic genes in Drosophila melanogaster. Nature . 1989;;337:468-471.
53 +
Zink B, Engstrom Y, Gehring WJ, Paro R.  Direct interaction of the polycomb protein with Antennapedia regulatory sequences in polytene chromosomes of Drosophila melanogaster. EMBO J . 1991;;10:153-162.
54 +
Paro R, Hogness DS.  The Polycomb protein shares a homologous domain with a heterochromatin-associated protein of Drosophila. Proc Natl Acad Sci U S A . 1991;;88:263-267.
55 +
Struhl G.  Genes controlling segmental specification in the Drosophila thorax. Proc Natl Acad Sci U S A . 1982;;79:7380-7384.
56 +
Struhl G, Akam M.  Altered distributions of Ultrabithorax transcripts in extra sex combs mutant embryos of Drosophila. EMBO J . 1985;;4:3259-3264.
57 +
Ingham PW, Whittle JRS.  Trithorax: a new homeotic mutation of Drosophila melanogaster causing transformations of abdominal and thoracic imaginal segments. J Mol Gen Genet . 1980;;179:607.
58 +
Ingham PW.  A new homeotic mutation of Drosophila melanogaster, II: the role of trx+ after embryogenesis. Wilhelm Rouxs Arch Dev Biol . 1981;;190:365.
59 +
McGinnis W, Levine M, Hafen E, Kuroiwa A, Gehring WJ.  A conserved DNA sequence found in homeotic genes of the Drosophila Antennapediaand bithorax complexes. Nature . 1984;;308:428-433.
60 +
Scott MP, Weiner AJ.  Structural relationships among genes that control development: sequence homology between the Antennapedia, Ultrabithorax, and fushi tarazu loci of Drosophila. Proc Natl Acad Sci U S A . 1984;;81:4115-4119.
61 +
Beeman RW.  A homeotic gene cluster in the red flour beetle. Nature . 1987;;327:247-249.
62 +
Beeman RW, Stuart JJ, Haas MS, Dennell RE.  Genetic analysis of the homeotic gene complex (HOM-C) in the beetle Tribolium castaneum. Dev Biol . 1989;;133:196-209.
63 +
Tsujita M.  On the crossing-over between EH and EK of the E allelic series in the silkworm. Jpn J Genet . 1955;;30:227-235.
64 +
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