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A Misexpression Study Examining Dorsal Thorax Formation in Drosophila melanogaster

A Misexpression Study Examining Dorsal Thorax Formation in Drosophila melanogaster
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  Copyright   ©  2002 by the Genetics Society of America  A Misexpression Study Examining Dorsal Thorax Formationin  Drosophila melanogaster  Marı´a Teresa Pen˜a-Rangel,* , † Isabel Rodriguez ‡ and Juan Rafael Riesgo-Escovar* , 1 *  Department of Developmental Neurobiology and Neurophysiology, Instituto de Neurobiologı ´ a, Universidad Nacional Auto ´ noma de Me ´ xico, Quere ´ taro, 76230, Me ´ xico,  †  Facultad de Ciencias Naturales, Universidad Auto ´ noma de Quere ´ taro, Quere ´ taro, 76010, Me ´ xico and   ‡ Centro de Biologia Molecular “Severo Ochoa,” Universidad Auto ´ noma de Madrid-Consejo Superior de Investigaciones Cientificas, 28049 Madrid, Espan ˜ a  Manuscript received October 11, 2001 Accepted for publication December 10, 2001 ABSTRACT We studied thorax formation in  Drosophila melanogaster   using a misexpression screen with EP lines andthoracic Gal4 drivers that provide a genetically sensitized background. We identified 191 interacting linesshowing alterations of thoracic bristles (number and/or location), thorax and scutellum malformations,lethality, or suppression of the thoracic phenotype used in the screen. We analyzed these lines and showedthat known genes with different functional roles (selector, prepattern, proneural, cell cycle regulation,lineage restriction, signaling pathways, transcriptional control, and chromatin organization) are amongthe modifier lines. A few lines have previously been identified in thorax formation, but others, such aschromatin-remodelingcomplexgenes,arenovel.However,mostoftheinteractinglociareuncharacterized,providing a wealth of new genetic data. We also describe one such novel line,  poco pelo   (  ppo  ), where bothmisexpression and loss-of-function phenotypes are similar: loss of bristles and scutellum malformation. G ENETIC screens for loss-of-function mutations mutations in other genes, especially those with whichthis gene interacts. To take advantage of a genetically havebeenconventionaltoolsfortheidentificationsensitized background while at the same time providingofgenesinmodelorganismslikeDrosophila( Nu¨sslein -a Gal4 driver line, we have employed mutant alleles of   Volhard  and  Wieschaus  1980). Unfortunately, early   pannier   (  pnr  ) and  apterous   ( ap  ), caused by insertionallethalityhindersstudiesoflaterfunctionsofthesegenes.mutagenesis as thoracic Gal4 driver lines ( Calleja  et   Also, redundancy or pleiotropy may prevent identifica- al.  1996).tion of many genes. In this regard,  Miklos  and  Rubin  pnr   is a pleiotropic gene that encodes a zinc-finger(1996) have estimated that two-thirds to three-quartersprotein with homology to vertebrate GATA transcrip-of all Drosophila genes have no obvious loss-of-functiontion factors ( Ramain  et al.  1993;  Winick  et al.  1993). Inmutantphenotypes.Inallthesecases,controlledtempo-embryos and larvae,  pnr   is expressed in dorsal tissuesral and spatial misexpression is an alternative for identi-(amnioserosa, lateral epidermis, and dorsal-most as-ficationofthesegenesandfacilitatesdescriptionoftheirpects of wing and eye imaginal discs). In adults,  pnr  genetic interactions.  Rørth (1996) devised a successfulexpression runs in a medial region from the head cap-system in Drosophila that allows controlled misexpres-sule to the posterior end of the abdomen ( Calleja  et  sionofgenesrandomlytaggedbyinsertionofatranspos- al.  1996).  pnr   functions as a prepattern gene requiredable element (EP element) containing UAS sites that forspecificationofthedorsocentralaspectofthethoraxcan bind the yeast transcripton factor Gal4 and a pro-together with  u-shaped   ( ush  ;  Haenlin  et al.  1997;moter directed outward 3   of the insertion site. Crosses Calleja  et al.  2000). Lateral aspects of the thorax areto lines bearing  gal4  -expressing insertions in definedspecified by another set of prepattern genes, the  iroquois  patterns allow misexpression of genes 3   of the EP ele-gene complex ( Go´mez - Skarmeta  et al.  1996). Null  pnr  ments in the progeny bearing both constructs.mutants are embryonic lethal with premature loss of the Very successful genetic screens have also been con-amnioserosa and defects in dorsal closure ( Heitzler  et  ducted in sensitized genetic backgrounds ( Simon  et  1996). Mutant clones in the notum anlagen of the1991;  Olivier  et al.  1993). In these cases, the genetic wing imaginal disc produce alterations in the patternbackground of the screen is not wild type, but containsof medial thoracic bristles and a strong dorsal thoracica mutation in a gene that “enhances” effects caused by cleft. The allele used in this study,  pnr  Gal4, has an inser-tion in the  pnr   promoter region that results in a hypo-morphic allele ( Calleja et al.  1996). Expression of Gal4 1 Corresponding author:   Department of Developmental Neurobiology, in  pnr  Gal4 closely mimics normal  pnr   expression. In Instituto de Neurobiologı´a, UNAM, Futbol #149, Col. Country Club heterozygous condition, adult   pnr  Gal4 flies show a very  Churubusco, Me´xico, D. F., 04220, Me´xico.E-mail:  slight dorsal thoracic cleft and disorganization of bris- Genetics  160:  1035–1050 (March 2002)  1036 M. T. Pen˜a-Rangel, I. Rodriguez and J. R. Riesgo-EscovarMATERIALS AND METHODS tles, sometimes missing a few inner and postverticalbristles (Figure 1B). Drosophila maintenance:  Fly stocks and crosses were main- These multiple functions of   pnr   allow several different   tained in cotton-stoppered glass vials in a molasses-yeast-gela-tin standard medium. phenotypes (and genes required for those phenotypes) Drosophila stocks:  The collection of EP transgenic lines to be screened for at the same time. We have exploited generated and described by   Rørth (1996) was obtained from this in our screen in order to identify genes required  J. Szabad at the European Drosophila stock center in Szeged, for bristle formation, thoracic closure, thorax and scu- Hungary, and from E. Hafen, University of Zu¨rich (Zurich, tellum shape, and viability.  Switzerland).  pnr   MD237 , the  pnr  Gal4 line ( Calleja  et al.  1996), was obtained from G. Morata, Autonomous University of Ma-  We also used  ap  Gal4 as a Gal4 driver counterscreen drid(Madrid,Spain). ap  Gal4andUAS-  pnr   wereobtainedfrom for some lines to allow us to separate effects due to the  J. Modolell, Autonomous University of Madrid. FRT-con- combination of particular sensitized backgrounds plus tainingchromosomesandtransgenichs-  flp  flieswereobtained misexpression  vs.  effects of misexpression alone . apter-  from E. Hafen, University of Zu¨rich. All other stocks used are ous   is a transcription factor harboring a LIM domain  described in  Lindsley  and  Zimm  (1992) or Flybase ( and a homeodomain that plays a key role in wing, halt- EP screen:  pnr  Gal4 virgin female flies were mated to males ere, and nervous system formation ( Cohen  et al.  1992; fromtheEPcollection.F 1 progenywerescoredunderadissect- Lundgren  et al.  1995). In larvae,  ap   is expressed in ing microscope for modification of the weak  pnr  Gal4/   phe- groups of cells of the dorsal compartment of the wing notype. As most EP lines represent insertions in the promoter disc, which also express  pnr  , and in the region giving  region of genes, we expected most of the effects observed tobe due to overexpression. A fraction of EP lines are inserted rise to the wing hinge and dorsal surface of the wing at the 3   end of genes, and so loss-of-function effects due to blade. We used a Gal4 allele of   ap   that drives Gal4 production of antisense transcripts could also be expected. expression in an  ap   expression pattern ( Calleja  et al.  All lines were tested with  pnr  Gal4 as driver, and some inter- 1996). Heterozygous adult   ap  Gal4 flies have wild-type acting lines were then tested with  ap  Gal4. All crosses were  wings and thorax.  carried out at 25  . Lines that modified the srcinal phenotype were retested at least once. In some cases, parents from initial The formation of complex structures like the Dro- crosses with a strong enhancement of the  pnr  Gal4 phenotype sophila thorax putatively requires a large number of   were retested at 25   and progeny were allowed to develop at  genes, including some involved in growth, differentia- 18  , 25  , and 29   to allow us to look for effects of different  tion, cellular death, and maintenance of the differenti- levels of expression of Gal4. ated state. Many genes that control these general pro-  AdultF 1 flieswithmodificationofthe  pnr  Gal4/  phenotype cesses are known. For example, growth of the wing  were fixed and stored in the dark in a 3:1 mixture of etha-nol:glycerol. Thoraxes of adult flies were viewed in stereo disc—the imaginal disc that gives rise to the thorax—is and optical microscopes (Nikon and Olympus) and digitally  controlledbyWingless(Wg),Hedgehog(Hh),mitogen- photographed (Optronics, Pixera). For scanning electron mi- activated protein kinase (MAPK), and Decapentaplegic croscopy, adult flies were fixed in 4% glutaraldehyde in phos- (Dpp) signaling pathways ( Clifford  and  Schu¨pbach  phate-buffered saline (PBS) for 2 hr at room temperature, 1989;  Blair  1995). Structures within the thorax, such  after ventral incisions in the thorax, abdomen, and head weremade. They were then washed in PBS and dehydrated in a asbristles,mayrequiredifferenttypesofgenes:selector, graded series of acetone-PBS (50, 70, and 100%) at room prepattern, and proneural genes for regional differenti- temperature. Afterward the specimens were critical point  ation, formation, and correct spacing, besides signaling dried, mounted in stubs dorsal thorax side up, sputter coated pathways. Dppand Wg arealso important forthe forma-  with gold, viewed, and photographed in a Zeiss scanning elec- tionofbristlesinthemesothorax( Tomoyasu etal. 1998;  tron microscope. Clonal analysis:  Mutant lethal alleles of   ppo   obtained by  Phillips  et al.  1999;  Sato  et al.  1999). Mutations in the imprecise  P  -element excisions were recombined onto FRT  Jun N-terminal kinase (JNK) pathway produce thoracic chromosomes. These  ppo   FRT chromosomes were crossed to clefts, indicating a failure in the coordination of imagi- appropriately marked FRT chromosomes with hs-  flp  , and heat  nal epithelial sheet spreading, a phenomenon similar shocks were applied to progeny larvae for 1 hr at 37   to gener- to dorsal closure during midembryogenesis ( Riesgo -  ate mutant clones in the thorax and wing. The larvae wereallowed to develop and examined as adults. We used  forked  Escovar  and  Hafen  1997;  Agne`s  et al.  1999;  Zeit- and  yellow   to mark clones. For the generation of germline linger  and  Bohmann  1999). Limited amounts of apo- clones, we followed the dominant female sterile technique of  ptosis also occur during thorax formation ( Milan  et al. Chou  and  Perrimon  (1996). 1997). In spite of this, very little is known about theactual overall genetic architecture that governs the for-mation of this structure. RESULTS AND DISCUSSION  We screened 2100 EP lines from which 191 (9%),For our screen, we hypothesized that lines where tho-corresponding to 167 loci, produced modifications of racic misexpression leads to alterations of the  pnr  Gal4the weak  pnr  Gal4 phenotype. These modifier lines iden-phenotype were candidate genes for thoracic develop-tifiedgenespreviouslyknowntobeimportantfornotumment. We found lines that modified the thorax/scutel-development, but also many novel and hitherto knownlum structure or that altered significantly the number,genesthatwerepreviouslynotcharacterizedasrequiredfor thoracic development. size,and/orarrangementofchaetesinthenotum.Over-  1037Dorsal Thorax Formation in Drosophila all modifications were produced in 9% of the 2100 lines cific two-dimensional patterns. This information is pro- vided by the prepattern ( Stern  1954), a combinationscreened. This compares favorably to other misexpres-sion screens ( Rørth  et al.  1998;  Abdelilah - Seyfried  of transcriptional activators and repressors distributedasymmetricallythatprefigurethepatternofeachregion et al.  2000;  Huang  and  Rubin  2000;  Kraut  et al.  2001),indicating that our screen was very sensitive. We classi- ( Campuzano and Modolell 1992).Onesuchtranscrip-tional repressor in the thoracic prepattern is Hairy.fied observed modifications in three broad categories:(1) enhancement of the  pnr  Gal4 phenotype in 5.9% Proneural genes are activated in groups of cells withinthese competent regions from which sensory organ pre-(125 of the total lines), (2) lethality (embryonic, larval,or pupal) in   1% (20 lines), and (3) suppression of cursorcellsorneuroblastswillform.Extramacrochaetae(Emc) act as antagonists to proneural gene functionthe  pnr  Gal4 phenotype in 2.1% (45 lines). The lines where the  pnr  Gal4 phenotype was enhanced showed: ( MoscosoDelPrado and Garcia - Bellido 1984; Ellis et al.  1990;  Garrell  and  Modolell  1990;  Ramain  et al. (a) modifications in the number and distribution of thoracic macrochaetes and/or microchaetes, (b) de- 1993). Prepatterns for bristle formation on the thoraxinvolve the establishment of a zone of competent cells,fects of the scutellum, and (c) formation of a cleft of  variable width and depth at the dorsal midline of the calledproneuralterritory,whereneuralprecursorsariseas sensory organ precursors (SOP).  emc   overexpressionthorax, with some lines showing more than one pheno-type. Very few lines modified the dorsal aspects of the gives rise to loss of SOPs ( Posakony  1994). InEP(3)0415, EP(3)3087, EP(3)3614, and EP(3)3620, thehead and abdomen (0.2%). Table 1 shows a summary of these results. Some modifier lines were retested and  P   element is inserted in the  emc   locus. Misexpression of these lines via  pnr  Gal4 resulted in complete loss of bris-progeny allowed to develop both at 18   and 29  . Prog-eny,except forlines EP(2)0639,EP(2)2148, EP(2)2402, tles in the  pnr   region (Table 1, Ic; Figure 1C), a result consistent with  emc   overexpression experiments. As inand EP(2)2437, showed similar phenotypes to thoseobserved at 25   (data not shown). These four lines have the previous case of   sd  , loss-of-function and misexpres-sion data support evidence of a gene’s requirement insertions in thesame locus and showedstronger effectsat 29  , including pupal lethality. for a function. This argues that relevant loci can beidentifiedthroughmisexpressionscreens,notwithstand-EP elements inserted in genes with previously knowneffects in the thorax acted as positive controls of the ing the caveat that misexpression can also yield arti-factual phenotypes.screen. In the following descriptions, we group genesfound in the screen by known function and use the  Cell cycle regulation genes:   Loss of bristles could alsoarise by alterations during the last stages of their forma-positive controls to validate results. Enhancement of the  pnr  Gal4/   phenotype: effects  tion, for example, by transformation of the support orexternal cells (the shaft or trichogen cell or the socket  on chaetae:  Selector genes:   The  scalloped   ( sd  ) gene is aselector gene that encodes a transcription factor ex- or tormogen cell) into neurons ( Posakony  1994) orloss of sensory mother cells ( Kimura et al.  1997), causedpressed in several imaginal discs, including the wingimaginal disc and the peripheral and central nervous by changes in the cell cycle or cell lethality. The EPelements in EP(3)3261 and EP(3)3426 are inserted insystems. Sd/Vestigial (Vg) heterodimers bind to  cis  -reg-ulatory sequences controlling patterns of gene expres-  string   ( stg  ), a gene that encodes a protein tyrosine phos-phatase involved in mitotic G2/M transition ( Edgar  et  sion for wing development ( Halder  et al.  1998). Inaddition, some mutant   sd   alleles have defects in the  al.  1994). We observed missing microchaetae in the  pnr  -expressing region with these lines (Table 1, Ia; Figureperipheral sense organs of the embryo ( Campbell  et al. 1992) and loss of sensory organs in the wing margin 1F).Conversely,asuppressionof   pnr  Gal4/  phenotype was observed with the EP(3)3432 line (Figure 1G). This( Campbell  et al.  1991). In our case, misexpression of  sd   via EP(X)1435, with both  pnr  Gal4 and  ap  Gal4, pro- line also contains an insertion in  string  , but in an anti-sense orientation, thus generating a loss-of-functionduced loss of several microchaetae and macrochaetae(Table 1, Ia; Figure 1D). In another gain-of-function phenotype.Reductionof  stg  expressionisseeningroupsofcellswheresensorymothercellsareemerging( Milan screen aimed at identifying genes required in externalsensory organ development, misexpression of   sd   using  et al.  1996), and  stg   hypomorphic combinations affect formationofmacrochaetae(  Verheyen etal. 1996).Again- sca  Gal4 also produced effects on bristles (  Abdelilah - Seyfried etal. 2000).Thesefindingsconfirmthatmisex- of-function study found that   stg   overexpression generatedtransformations of shaft to socket cells (  Abdelilah - Sey- pression of  sd  , irrespective ofGal4 driver orof sensitizedbackground, alters numbers of microchaetae.  sd   mu-  fried  et al.  2000).Misexpression of several other lines such as EP(2)1221,tants have chemosensory defects (  Anand  et al.  1990).Taken together, these data argue for a function of   sd   EP(2)2356,EP(3)3072,EP(3)3073,EP(3)3306,andEP(3)3621 also results in loss of bristles. These insertions arein bristle formation, perhaps in conjunction with othertranscription factors like Vg. in four different novel genes (see Table 1, Ia). Effects on the scutellum:  Lineage restriction genes:   The Prepattern and proneural genes:   Precise positional infor-mationis requiredduringdevelopmentto generatespe- epidermis of imaginal discs is divided into anterior and  1038 M. T. Pen˜a-Rangel, I. Rodriguez and J. R. 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    E    P    (    2    )    2    3    5    6 ,    5    7    A    5  -    A    6     l    (    2    )    k    0    0    9    9    2    0     L   o   s   s   o    f   m   a   c   r   o   c    h   a   e   t   a   e   a   n    d   m    i   c   r   o   c    h   a   e   t   a   e    i   n    d   o   r   s   a    l    L   o   s   s   o    f   e   x   t   e   r   n   a    l   c   e    l    l   s    2    5    8    6   m    i    d    l    i   n   e    E    P    (    2    )    2    5    3    5    4    5    C    4    L    D    2    0    8    9    2    D   e    f   o   r   m   e    d   m   a   c   r   o   c    h   a   e   t   a   e    E    P    (    2    )    2    6    1    9    4    7    C    1  -    C    2    L    D    0    8    7    1    7    M    i   c   r   o   c    h   a   e   t   a   e   w    i   t    h   o   u   t   p   o    l   a   r    i   t   y    E    P    (    3    )    3    0    7    2    6    5    A    6    L   o   s   s   o    f   r   o   w   o    f   m    i   c   r   o   c    h   a   e   t   a   e    i   n   t    h   e    d   o   r   s   a    l   m    i    d    l    i   n   e    E    P    (    3    )    3    0    7    3    9    2    E  -    F    L    D    0    5    5    3    0    L   o   s   s   o    f   s   e   v   e   r   a    l    d   o   r   s   o   c   e   n   t   r   a    l   m    i   c   r   o   c    h   a   e   t   a   t   e    L   o   s   s   o    f   e   x   t   e   r   n   a    l   c   e    l    l   s    E    P    (    3    )    3    0    8    7 ,    6    1    D   e  x   t  r  a  m  a  c  r  o  c    h  a  e   t  a  e     C   o   m   p    l   e   t   e    l   o   s   s   o    f    d   o   r   s   o   c   e   n   t   r   a    l   a   n    d   s   c   u   t   e    l    l   a   r   m   a   c   r   o  -    3    6    2    0 ,    3    6    1    4 ,   c    h   a   e   t   a   e   a   n    d   m    i   c   r   o   c    h   a   e   t   a   e    i   n    d   o   r   s   a    l   m    i    d    l    i   n   e    i   n  -    0    4    1    5 ,    3    1    6    6   c    l   u    d    i   n   g   t    h   e   a    b    d   o   m   e   n    E    P    (    3    )    3    2    6    1 ,    9    9    A    6   s   t  r    i  n  g     L   o   s   s   o    f    d   o   r   s   o   c   e   n   t   r   a    l   m   a   c   r   o   c    h   a   e   t   a   e   a   n    d   s   e   v   e   r   a    l   m    i  -    P   o   t   e   n   t    i   a    l   c   e    l    l    f   a   t   e    3    4    2    6   c   r   o   c    h   a   e   t   a   e .    S   o   m   e   s    h   o   r   t   m   a   c   r   o   c    h   a   e   t   a   e   t   r   a   n   s    f   o   r   m   a   t    i   o   n   s    E    P    (    3    )    3    3    0    6    L   o   s   s   o    f    d   o   r   s   o   c   e   n   t   r   a    l   m   a   c   r   o   c    h   a   e   t   a   e   a   n    d   s   e   v   e   r   a    l   m    i  -   c   r   o   c    h   a   e   t   a   e    E    P    (    3    )    3    4    4    9    9    3    F    4  -    F    5     G    l    i  o    l  e  c   t    i  n     L   o   s   s   o    f   s   c   u   t   e    l    l   a   r   m   a   c   r   o   c    h   a   e   t   a   e   a   n    d    f   r   e   q   u   e   n   t    l   o   s   s   o    f    L   o   s   s   o    f   e   x   t   e   r   n   a    l   c   e    l    l   s    d   o   r   s   o   c   e   n   t   r   a    l   m   a   c   r   o   c    h   a   e   t   a   e    E    P    (    3    )    3    6    2    1    7    0    B    3  -    B    4    L   o   s   s   o    f    d   o   r   s   o   c   e   n   t   r   a    l   a   n    d   s   c   u   t   e    l    l   a   r   m   a   c   r   o   c    h   a   e   t   a   e   a   n    d    l   o   s   s   o    f   m    i   c   r   o   c    h   a   e   t   a   e    E    P    (    3    )    0    6    3    2    8    5    D    1    0     l    (    3    )    L    4    0    9    2     E   x   t   r   a   s   c   u   t   e    l    l   a   r   m   a   c   r   o   c    h   a   e   t   a   e    [   s   e   e    E    P    (    3    )    3    6    9    0 ,   s   e   c  -   t    i   o   n    1    d    ]    E    P    (    2    )    0    8    4    5    5    3    F    1    1     l    (    2    )    k    0    8    8    0    5     E   x   t   r   a   s   c   u   t   e    l    l   a   r   m   a   c   r   o   c    h   a   e   t   a   e    E    P    (    3    )    0    9    0    6    6    5    F    4    E   x   t   r   a   s   c   u   t   e    l    l   a   r   m   a   c   r   o   c    h   a   e   t   a   e    E    P    (    3    )    0    9    1    5    E   x   t   r   a   s   c   u   t   e    l    l   a   r   m   a   c   r   o   c    h   a   e   t   a   e    E    P    (    3    )    0    9    2    4    7    3    E    4    E   x   t   r   a   s   c   u   t   e    l    l   a   r   m   a   c   r   o   c    h   a   e   t   a   e    E    P    (    2    )    1    0    2    0    2    3    C    1  -    C    2    G    M    0    6    0    7    0   a   n    d   o   t    h   e   r   s    E   x   t   r   a   s   c   u   t   e    l    l   a   r   m   a   c   r   o   c    h   a   e   t   a   e    E    P    (    3    )    1    0    3    7    9    1    A    2    E   x   t   r   a   s   c   u   t   e    l    l   a   r   m   a   c   r   o   c    h   a   e   t   a   e    E    P    (    2    )    1    0    6    2    5    0    B    6  -    B    7    E   x   t   r   a   s   c   u   t   e    l    l   a   r   m   a   c   r   o   c    h   a   e   t   a   e    E    P    (    2    )    1    0    6    5    6    0    E    1  -    E    2     R  e  g  -    5     E   x   t   r   a   s   c   u   t   e    l    l   a   r   m   a   c   r   o   c    h   a   e   t   a   e    E    P    (    3    )    1    0    8    2    8    5    D    2    5    C    G    1    6    7    8    8    E   x   t   r   a   s   c   u   t   e    l    l   a   r   m   a   c   r   o   c    h   a   e   t   a   e    (   c  o  n   t    i  n  u  e    d     )  1039Dorsal Thorax Formation in Drosophila     T    A    B    L    E    1    (    C   o   n    t    i   n   u   e    d    )     M    i   s   e   x   p   r   e   s   s    i   o   n   p    h   e   n   o   t   y   p   e    M    i   s   e   x   p   r   e   s   s    i   o   n   p    h   e   n   o   t   y   p   e    M    i   s   e   x   p   r   e   s   s    i   o   n   p    h   e   n   o   t   y   p   e    i   n    E    P    l    i   n   e    M   a   p   p   o   s    i   t    i   o   n    G   e   n   e   w    i   t    h    p  n  r     G   a    l    4    /           w    i   t    h   a   p     G   a    l    4    /             A    b    d    e    l    i    l    a    h  -     S    e    y    f    r    i    e    d   e   t  a    l  .    (    2    0    0    0    )    E    P    (    X    )    1    0    9    3    9    E    1  -    E    2    L    D    0    6    8    2    5   a   n    d    E   x   t   r   a   s   c   u   t   e    l    l   a   r   m   a   c   r   o   c    h   a   e   t   a   e    L    D    0    2    6    7    3    E    P    (    3    )    1    1    1    3    7    6    D    7    E   x   t   r   a   s   c   u   t   e    l    l   a   r   m   a   c   r   o   c    h   a   e   t   a   e    E    P    (    X    )    1    1    2    5    2    F    4  -    F    5    E   x   t   r   a   s   c   u   t   e    l    l   a   r   m   a   c   r   o   c    h   a   e   t   a   e    E    P    (    2    )    1    1    3    9    4    9    B    1    0    E   x   t   r   a   s   c   u   t   e    l    l   a   r   m   a   c   r   o   c    h   a   e   t   a   e    E    P    (    3    )    1    1    5    4    8    3    C    2    E   x   t   r   a   s   c   u   t   e    l    l   a   r   m   a   c   r   o   c    h   a   e   t   a   e    E    P    (    X    )    1    3    0    6    1    7    C    1  -    C    4     b  e  a    d  e  x     E   x   t   r   a   s   c   u   t   e    l    l   a   r   m   a   c   r   o   c    h   a   e   t   a   e .    L   o   s   s   o    f   e   x   t   e   r   n   a    l   c   e    l    l   s    [    S   e   e    E    P    (    X    )    1    3    8    3 ,    1    3    9    4 ,   s   e   c   t    i   o   n    1    d    ]    E    P    (    X    )    1    6    4    4    1    8    A    1  -    A    2    L    D    1    5    4    0    4    E   x   t   r   a   s   c   u   t   e    l    l   a   r   m   a   c   r   o   c    h   a   e   t   a   e    E    P    (    2    )    2    0    8    6    3    8    E    6    E   x   t   r   a   s   c   u   t   e    l    l   a   r   m   a   c   r   o   c    h   a   e   t   a   e    E    P    (    2    )    2    5    2    3    5    3    D    1    3     l    (    2    )    k    0    9    9    0    7    a   n    d    E   x   t   r   a   s   c   u   t   e    l    l   a   r   m   a   c   r   o   c    h   a   e   t   a   e   o   t    h   e   r   s    E    P    (    2    )    2    5    9    5    2    4    C    1  -    C    2    E   x   t   r   a   s   c   u   t   e    l    l   a   r   m   a   c   r   o   c    h   a   e   t   a   e    E    P    (    3    )    3    1    8    6    9    1    F    7    E   x   t   r   a   s   c   u   t   e    l    l   a   r   m   a   c   r   o   c    h   a   e   t   a   e    E    P    (    3    )    3    2    4    6    8    5    B    2    G    H    0    4    5    1    7   a   n    d   o   t    h   e   r   s    E   x   t   r   a   s   c   u   t   e    l    l   a   r   m   a   c   r   o   c    h   a   e   t   a   e    E    P    (    3    )    3    3    9    0    9    8    F    1    0    E   x   t   r   a    d   o   r   s   o   c   e   n   t   r   a    l   o   r   s   c   u   t   e    l    l   a   r    P   o   t   e   n   t    i   a    l   c   e    l    l    f   a   t   e   m   a   c   r   o   c    h   a   e   t   a   e   t   r   a   n   s    f   o   r   m   a   t    i   o   n   s    (    b    )    E    f    f   e   c   t   s   o   n   t    h   e   s   c   u   t   e    l    l   u   m    E    P    (    X    )    0    3    8    5    1    2    B    1  -    B    2    R    E    3    7    1    8    6    N   o   s   c   u   t   e    l    l   u   m    f   o   r   m   e    d    E    P    (    X    )    0    4    4    3    1    7    C    1  -    C    2     b  e  a    d  e  x     R   e    d   u   c   e    d   s   c   u   t   e    l    l   u   m    [   s   e   e    E    P    (    X    )    1    3    0    6 ,   s   e   c   t    i   o   n    1   a    ]    E    P    (    3    )    0    6    6    6    8    8    D    1  -    D    2    R    E    2    6    3    5    0   a   n    d   o   t    h   e   r   s    R   e    d   u   c   e    d   s   c   u   t   e    l    l   u   m    S    l    i   g    h   t    l   y    d   e    f   o   r   m   e    d   s   c   u   t   e    l  -    l   u   m    E    P    (    3    )    0    7    0    7    8    5    D    1    5    D   e    f   o   r   m   e    d   s   c   u   t   e    l    l   u   m    E    P    (    2    )    0    8    5    3    2    3    C    4  -    C    5    R    E    6    0    9    8    6    R   e    d   u   c   e    d   s   c   u   t   e    l    l   u   m    E    P    (    2    )    0    9    4    1    4    4    D    5  -    D    6    p  a   t  c    h  e    d     N   o   s   c   u   t   e    l    l   u   m    f   o   r   m   e    d    E    P    (    2    )    1    2    2    0    2    1    B    5   s  m  o  o   t    h  e  n  e    d     D   e    f   o   r   m   e    d   s   c   u   t   e    l    l   u   m    E    P    (    2    )    1    2    3    6    5    3    F    1    1    R   e    d   u   c   e    d   s   c   u   t   e    l    l   u   m    E    P    (    3    )    1    2    4    6    6    9    E    1    D   e    f   o   r   m   e    d   s   c   u   t   e    l    l   u   m    E    P    (    X    )    1    3    4    0    7    A    1  -    A    2    D   e    f   o   r   m   e    d   s   c   u   t   e    l    l   u   m    E    P    (    X    )    1    3    5    0    1    6    A    1  -    A    2    H   o   m   o    l   o   g   y   w    i   t    h    D   e    f   o   r   m   e    d   s   c   u   t   e    l    l   u   m    B   a   r    H    2    E    P    (    2    )    2    4    1    9    2    8    B    1  -    B    2    D   e    f   o   r   m   e    d   s   c   u   t   e    l    l   u   m    E    P    (    2    )    2    4    3    3    3    0    C    2    R   e    d   u   c   e    d   s   c   u   t   e    l    l   u   m    E    P    (    3    )    3    0    6    0    8    4    C    6    R    E    5    2    3    9    3   a   n    d   o   t    h   e   r   s    R   e    d   u   c   e    d   s   c   u   t   e    l    l   u   m    E    P    (    3    )    3    1    4    5    8    8    F    4    G    H    2    7    0    2    9   a   n    d    D   e    f   o   r   m   e    d   s   c   u   t   e    l    l   u   m   o   t    h   e   r   s    E    P    (    3    )    3    1    9    6    8    9    E    1    0  -    E    1    1    D   e    f   o   r   m   e    d   s   c   u   t   e    l    l   u   m    E    P    (    3    )    3    6    6    2    9    3    F    4    R    E    5    6    0    6    1   a   n    d   o   t    h   e   r   s    D   e    f   o   r   m   e    d   s   c   u   t   e    l    l   u   m    (   c  o  n   t    i  n  u  e    d     )
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