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Molecular Aspects of Genetic Recombination and Their Relevance to Cutaneous Biology* D

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Molecular Aspects of Genetic Recombination and Their Relevance to Cutaneous Biology* D THE JOURNAL OF I NVESTIGATI VE DERMATOLOGY Vol. 60, No. G Copy rig h t@ 1973 by The Will iams & Wilkins Co. Printed in U.S.A. MOLECULAR ASPECTS OF GENETIC RECOMBINATION AND THEIR RELEVANCE TO CUTANEOUS BIOLOGY* D. MARTIN CARTER, M.D., PH.D. t INTRODUCTION spaced. In " fin e-structure" mapping, recom bina­ Through ge netic recombination, a fundam ental tiO n fr equency is considered a fu nction of t he biologic process t hat reassorts linked ue netic distance between recombining markers (Benze r, markers, offspring can ex press ge netic traits t hat 1961 ). Genetic maps actuall y re present t he linear were not present together in either parent. Ind i­ structure of t he DNA molec ule. T he agreement vidual progeny may be mult ice llul ar orua nisms between ge netic maps a nd t he physical distance single cell s, bacteria, viruses, or molebc ul es oi· along t he DNA mo lecul e is ve ry high in bacteria DNA. To medical biologists, recombination is and bacteriophage (Hogness et al. , 1966). At t he usually identifi ed with the process of crossin rr-ove r present t ime, recombination data from hi rr her in w hic h genetic material i s exchanged b etween organisms are much less helpful in definin ub t he homologous chromosomes durinu meiosis. Genetic process in molecul ar terms. T his may r e fl ect~ less recombination is now f elt to bhave even wid er precise knowledge of eukaryotic chromosome significa n ce, having been implicated in such di­ structure regarding t he li near red upl ication of verse biologic phenomena as the circul ari zation of genes and whether all DNA is fun ctional (Call an, the b acteri al chromosome before repli cation t he 1967; T homas, 1970). It wo uld be naiv e to assume insertion of t he DNA of temperate viruses' in to t hat all organisms perform recombination in an host D A , DNA-mediated b acteri al transforma­ identical m a nner, a nd distinctions between organ­ tion , and as t he ge neral m eans by whi ch ue netic Isms have a lready been delineated. However it var iability is generated (see reviews by Bodmer is ge nerally assumed that t he mechanism f or 'all and Darlington, 1969; Davern , 1971). recombination events, in all species, preserves many co mmon features. Whatever m odel is de­ GENE FUNCTION IN RECOMBINATION: A REFLECTION vised f or r eco mbination, it must accoun t for at OF DNA STRUCTURE least t':"o characteristic features of t he process: synapsts, the a li gnment or pai ring of homologous U nderstanding t he organi zation of t he DNA chromosome segments; and exchange, t he recom­ molecule, we can co rre late rather precisely t h e bining o f information h eld in DNA of t he homo­ chemical structure of the materi al storinu ue netic logs . information with some of t he ge netic e~e~1ts af­ fecting t he ex pression of t his information . BREAKING AN D HEJOINI NG VERSUS COPY CHOICE Chromosomes, which co ntain ge nes in a linear For many years, two array, are composed primarily o f D NA. The well ­ classic t heori es for recom­ b~nati o n vied for acceptance . Breaking known dou ble heli x can be depicted in a number and joining of homologous molec of ways (Fig. 1). Repeating spirals can s imulate ul es. a t heo ry origin all y pro­ posed b y J anssens ( the t hree-dimensiona l structure o f t he ri gid DNA 1909), was proposed to explain cytologic observations of m molec ule (la), or the molecule can be opened-out eiotic chi asmata. J ans­ sens suggested t hat chr diagrammaticall y, to reveal t he covalently linkecl omoso mal coiling produced sufficient tension to suga r-phos phate " backbone" of each strand and break chromatids and that homologs rejoined to the h ydrogen-bonded pairs of nucleotides holdinu produce reciprocally recom­ binan t proge the t wo strands together ( 1c). Further abbrev i a~ ny. J anssens' model could not ade­ quately account for t tion can reduce a diagram of t he DNA molecul e to he pa iring of DNA molecules; but even more t roubleso me, since two lines with cross-li nks (1b). Each of t hese chromosome s ize is constant, was diagrams s hows t hat t h"e intact molec ul e co ntains its require ment t hat a me­ chani cal process should two complementary polynucleotide c hains of op­ produce breaking o f ho­ mologous chromatids at prec isely t h posite pol a rity held together b y hydrogen b onds. e same in ter­ nucleot id e sites. _Ge net ic. ma ps _have been constructed f or many Another model, known as copy microrganisms from studies of t he freq uency choice was ori gin all y s uggested b y Belling (1931). He !'inked with which r ecombinant progeny occur in crosses recombination wi t h chromosome repli catio between parents with all eli c markers at adjacent n so that only the in fo rmation of both parents, but not or far-spaced sites on t he c hromosome. There is t he actual parental D NA , would be linked in the less crossing over between mutations located close DNA of recombinant pr togeth er t han b etween t hose more distantly ogeny. T he model suggests that an enzyme, DNA polymerase, cha nges pa­ This work was s upported in part by USP HS Grant. rental template when synthesizin g re co mbina nt ·a. ROl C A 12496-01. molecul es. T he major difference between these . • From t h e D epartment or Derm atology, Ya le Uni ve r­ stty School of Med1c1ne, New Have n, Co nn ecticut . two models is t he importance attached to DNA . t Howard Hughes Medi cal Investigator, Yale Uni ve r­ repli cation: t he co py c hoice t heo ry is completely Si ty. dependent upon DNA replication wh ereas t he 369 370 THE JOURNAL OF INVESTIGATIVE DERMATOLOGY (a) 3' 5' (b) 5' 3' cha ins; (2) pairing homologous segmen ts; (3) repairing t he recombina nt molecule by trimming excess DNA a nd fill ing in missing sequen ces; a nd (4) closing t he polynucleotide chain (Table I ). The a bove should be viewed as t he sine qua non of recombination but not necessarily a ll t he steps fo r whi ch every conceivabl e molecular m odel must m ake provision . 3' 5' ® 5' Enzymes for Breahing and J oining le i ® ,--(" (d) p~ :: ~® The growin g number of enzymes from variou biologic systems t hat are capable of acting upon ®Y)----@ : : c ,-{"" r .. ~® different kinds of DNA s ubstrates (Richardson . 1969) provides t he tools with which molecula r ®~ :: tB-C(® model building can proceed. Acting under their specified condit ions upon the backbone of t he ,---{" ®~c ::~-· ® DNA molecul e, the various nucleases, polymer­ 5' ® ases, a nd li gases can break or rejoin the suga r­ 3' 5' phosphate linkages between adjacent nucleotides FIG. l. Diagramatic representations o f the double (Fig. 2) . Table I shows how t hese enzymic acti\'i­ helic al structure of DNA . A = adenine, T = thymine, G ties might contribute to recombination b y brea k­ = guanine, C = cytosin e; 5' and 3' refer to the polarity of ing a nd rejoining. Figure 3 represents the kind of the suga r-ph os phate backbone. theorizing engaged in by a number of con tempo­ rary biologists (e.g., Thomas, 1966; Meselson. breaking a nd joining theory is not. M eselson and 1967; a nd Whitehouse, 1968). others using de nsity gradient techniques demon­ The sorts of enzymi c properties required for strated t h at recombinant progeny of phage recombination b y breaking a nd rejoining mig h t be la mbda can be composed almost ent irely of pa­ expected to participate in other biologic processes ren tal materia l (Meselson and Weigle, 1961; Kel­ affecting D NA. Best known of these are DNA lenberger et aL, 1961) and clearl y establi shed that re plication and t he repair of injuries to DNA recombina nt progeny DN A m olecules can be pro­ induced by ult raviolet light . Among t he fi rst duced by t he breaking and rejoining of parental recom bination-defective mutants iden tified for E. D N A. S ubsequent studies of phage lambda co li were those fr om a g roup of organisms excep­ showed that extens ive new DNA synthesis can tionally sensit ive to irradia tion by ul traviolet light also accompa ny breaking a nd rejoining in recom­ (Howa rd -Fla nders a nd Theriot, 1966). Among t he bination (Stahl a nd Stahl, 197 1). few enzymes known to be required for recombina­ t ion are those listed in Table II. These have b een THE H YBRID OVERLAP AND SYNAPSIS id ent ifi ed from careful genetic a n d biochemical Breaking a nd joining of DNA can t hus explain evaluation of recombination defective mutant m t he exchange step in recombination, but what several microorganis ms . m echanism has sufficient precision to keep the m olecular size of progeny molecules constant? The Reco mbination Enzym es of Phage Lambda What permits the prec ise pairing of DNA in The clearest data establis hing a certain enzymic syn a psis before excha nge? Double-stranded DNA activity with recombination h ave been gath ered molecules would not be expected to ali gn chemi­ for phage la mbda .
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