Cellular Regulation Of Natural Genetic Engineering

(Ebina and Levin 2007; Mittelman, Sykoudis et al. 2010; Mittelman and Wilson 2010; Hua-Van, Le Rouzic et al. 2011; Nagai, Davoodi et al. 2011; Newton and Bordenstein 2011; Vitale, Galluzzi et al. 2011)

 

Control of replication proofreading, repair and recombination functions (including mutator polymerases)

 

(Darmon, Lopez-Vernaza et al. 2007; Thorslund and West 2007; Cohen, Godoy et al. 2009; Galhardo, Do et al. 2009; Heidelberg, Nelson et al. 2009; Chen, Liu et al. 2010; Chen, Liu et al. 2010; Cohen, Lewis et al. 2010; Frisch, Su et al. 2010; Koskiniemi, Hughes et al. 2010; Wallace, Belancio et al. 2010; Cohen and Walker 2011; Debora, Vidales et al. 2011; Kang, Reardon et al. 2011; Lippert, Kim et al. 2011; Liu, Renault et al. 2011; Mischo, Gomez-Gonzalez et al. 2011; Storvik and Foster 2011; Takahashi, Burguiere-Slezak et al. 2011; Vader, Blitzblau et al. 2011)

 

Prokaryotic CRISPRs

 

(Bolotin, Quinquis et al. 2005; Haft, Selengut et al. 2005; Makarova, Grishin et al. 2006; Barrangou, Fremaux et al. 2007; Andersson and Banfield 2008; Beloglazova, Brown et al. 2008; Brouns, Jore et al. 2008; Carte, Wang et al. 2008; Deveau, Barrangou et al. 2008; Horvath, Romero et al. 2008; Sorek, Kunin et al. 2008; Vestergaard, Shah et al. 2008; Horvath, Coute-Monvoisin et al. 2009; Makarova, Wolf et al. 2009; Narberhaus and Vogel 2009; Rousseau, Gonnet et al. 2009; Shah, Hansen et al. 2009; van der Oost and Brouns 2009; van der Oost, Jore et al. 2009; van der Ploeg 2009; Wiedenheft, Zhou et al. 2009; Garneau, Dupuis et al. 2010; Haurwitz, Jinek et al. 2010; Horvath and Barrangou 2010; Sorokin, Gelfand et al. 2010; Sorokin, Gelfand et al. 2010; Al-Attar, Westra et al. 2011; Blower, Pei et al. 2011; Deltcheva, Chylinski et al. 2011; Garrett, Shah et al. 2011; Jore, Lundgren et al. 2011; Makarova, Aravind et al. 2011; Makarova, Haft et al. 2011; Makarova, Wolf et al. 2011; Semenova, Jore et al. 2011; Terns and Terns 2011; Wiedenheft, Lander et al. 2011)

 

RNA interference and epigenetic regulation in eukaryotes directed by piRNAs and other RNA molecules

 

(Dalmay, Hamilton et al. 2000; Miura, Yonebayashi et al. 2001; Kubis, Castilho et al. 2003; Sijen and Plasterk 2003; Sollars, Lu et al. 2003; Baulcombe 2004; Xie, Johansen et al. 2004; Kalmykova, Klenov et al. 2005; Onodera, Haag et al. 2005; Karpinets, Greenwood et al. 2006; Zambon, Vakharia et al. 2006; Brennecke, Aravin et al. 2007; Dramard, Heidmann et al. 2007; Murchison, Stein et al. 2007; Brennecke, Malone et al. 2008; Casas-Mollano, Rohr et al. 2008; Desset, Buchon et al. 2008; Devor, Huang et al. 2008; Girard and Hannon 2008; Pikaard, Haag et al. 2008; Siomi 2008; Chen 2009; Daxinger, Kanno et al. 2009; Halic and Moazed 2009; Huda and Jordan 2009; Jia, Lisch et al. 2009; Klattenhoff, Xi et al. 2009; Malone and Hannon 2009; Michalak 2009; Mourier and Willerslev 2009; Narberhaus and Vogel 2009; van der Heijden and Bortvin 2009; van Rij and Berezikov 2009; Cantu, Vanzetti et al. 2010; Huda, Marino-Ramirez et al. 2010; Khurana and Theurkauf 2010; Kirino, Vourekas et al. 2010; Nowacki, Haye et al. 2010; Patil and Kai 2010; Siomi, Mannen et al. 2010; Siomi, Miyoshi et al. 2010; Specchia, Piacentini et al. 2010; Takacs, Banati et al. 2010; De Fazio, Bartonicek et al. 2011; Gangaraju, Yin et al. 2011; Huda, Bowen et al. 2011; Ito, Gaubert et al. 2011; Kibanov, Egorova et al. 2011; Rigal and Mathieu 2011; Xie, Liang et al. 2011)

 

DNA transposons

 

(Fischer, van Luenen et al. 1999; Timakov, Liu et al. 2002; Chung, Okamura et al. 2008; O'Donnell and Boeke 2008; Rozhkov, Aravin et al. 2010; Wang, Wang et al. 2010; Guerreiro 2011)

 

Retrotransposons           

 

(Neumann, Yan et al. 2007; Siomi, Saito et al. 2008; Faulkner, Kimura et al. 2009; Guerreiro 2011)

 

            Retrovirus and LTR retrotransposons: (Errede, Company et al. 1985; Company and Errede 1987; Fulton, Rathjen et al. 1988; Bradshaw and McEntee 1989; Scheinker, Lozovskaya et al. 1990; Dupressoir and Heidmann 1996; Grandbastien, Lucas et al. 1997; Ke, Irwin et al. 1997; Takeda, Sugimoto et al. 1998; Kimura, Tosa et al. 2001; Barbot, Dupressoir et al. 2002; Scholes, Kenny et al. 2003; Sacerdot, Mercier et al. 2005; Sehgal, Lee et al. 2007; Cam, Noma et al. 2008; Desset, Buchon et al. 2008; Labrador, Sha et al. 2008; Saito, Keng et al. 2008; Mourier and Willerslev 2009; Brunmeir, Lagger et al. 2010; Kaneko-Ishino and Ishino 2010; Lu, Contreras et al. 2011)

 

            Non-LTR retrotransposons: (Busseau, Chaboissier et al. 1994; de La Roche Saint Andre and Bregliano 1998; Labrador, Farre et al. 1999; Gauthier, Tatout et al. 2000; Tchenio, Casella et al. 2000; Li and Schmid 2001; Yu, Zingler et al. 2001; Hagan, Sheffield et al. 2003; Dimitri and Bucheton 2005; Kale, Moore et al. 2005; Dramard, Heidmann et al. 2007; Garcia-Perez, Doucet et al. 2007; Goodier, Zhang et al. 2007; Perrin, Ballestar et al. 2007; Ramos, He et al. 2007; van den Hurk, Meij et al. 2007; Eickbush, Ye et al. 2008; Ogino, Kawasaki et al. 2008; Wallace, Wagstaff et al. 2008; Yamamoto, Toyota et al. 2008; Montoya-Durango, Liu et al. 2009; Muotri, Zhao et al. 2009; Saito, Suzuki et al. 2009; Zhou and Eickbush 2009; Wallace, Belancio et al. 2010; De Fazio, Bartonicek et al. 2011; Macia, Munoz-Lopez et al. 2011; Yoshida, Yamashita et al. 2011)

 

Hybrid dysgenesis & interspecific hybridization

 

(Bregliano 1983; Kidwell 1985; Fawcett, Lister et al. 1986; Kocur, Drier et al. 1986; Yannopoulos, Stamatis et al. 1987; Kidwell, Kimura et al. 1988; Bucheton 1990; Scheinker, Lozovskaya et al. 1990; Petrov, Schutzman et al. 1995; Vieira, Vieira et al. 1998; Labrador, Farre et al. 1999; Sundararajan, Atkinson et al. 1999; Vrana, Fossella et al. 2000; Moschetti, Dimitri et al. 2010; Wang, Wang et al. 2010)

 

Effects of genome doubling, karyotypic changes and nuclear structure components

(Chen and Ni 2006; Chen 2007; Goodier, Zhang et al. 2007; Gonzalez-Suarez, Redwood et al. 2009; Gonzalez-Suarez and Gonzalo 2010)

 

Genome position effects on mobile elements and repeat-induced point mutation (RIP)

(Galagan and Selker 2004; Hood, Katawczik et al. 2005; Crouch, Glasheen et al. 2008; Kojima and Kanehisa 2008; Lewis, Honda et al. 2009; Esnault, Palavesam et al. 2011; Rouxel, Grandaubert et al. 2011)

Adaptive Mutation

(Shapiro 1984; Cairns, Overbaugh et al. 1988; Shapiro and Leach 1990; Foster 1993; Maenhaut-Michel and Shapiro 1994; Shapiro 1994; Bridges 1995; Hall 1997; Maenhaut-Michel, Blake et al. 1997; Shapiro 1997; Torkelson, Harris et al. 1997; Lamrani, Ranquet et al. 1999; Lombardo, Torkelson et al. 1999; Bull, McKenzie et al. 2000; Godoy and Fox 2000; McKenzie, Harris et al. 2000; Bjedov, Tenaillon et al. 2003; Cairns and Foster 2003; Kivisaar 2003; Layton and Foster 2003; Tompkins, Nelson et al. 2003; Hastings, Slack et al. 2004; Heidenreich, Holzmann et al. 2004; Hersh, Ponder et al. 2004; Ilves, Horak et al. 2004; Roth and Andersson 2004; Zeyl 2004; Badyaev 2005; Erill, Campoy et al. 2006; He, Rohatgi et al. 2006; Karpinets, Greenwood et al. 2006; Kugelberg, Kofoid et al. 2006; Roth, Kugelberg et al. 2006; Slack, Thornton et al. 2006; Foster 2007; Hastings 2007; Heidenreich 2007; Robleto, Yasbin et al. 2007; Stumpf, Poteete et al. 2007; Williams and Foster 2007; Chodavarapu, Gomez et al. 2008; Gonzalez, Hadany et al. 2008; Jung and Kim 2008; Galhardo, Do et al. 2009; Goodarzi, Hottes et al. 2009; Petrosino, Galhardo et al. 2009; Vidales, Cardenas et al. 2009; Cohen and Walker 2010; Frisch, Su et al. 2010; Gibson, Lombardo et al. 2010; Kugelberg, Kofoid et al. 2010; MacPhee and Ambrose 2010; Ninio 2010; Pybus, Pedraza-Reyes et al. 2010; Debora, Vidales et al. 2011; Lin, Gibson et al. 2011; Lippert, Kim et al. 2011; Quinones-Soto and Roth 2011; Shee, Gibson et al. 2011; Storvik and Foster 2011)

Ciliate macronuclear development

(Juranek and Lipps 2007; Postberg, Heyse et al. 2008; Heyse, Jonsson et al. 2010)

Antiviral functions

(Villarreal 2011; Wang, Villion et al. 2011)

 

Table II.7. Various stimuli documented to activate natural genetic engineering.

Signal or condition

Natural genetic engineering function

Organism(s)

Reference

Quorum pheromones

DNA release and competence for DNA uptake

Multiple bacteria

(Miller and Bassler 2001; Sturme, Kleerebezem et al. 2002; Spoering and Gilmore 2006)

Chitin

Competence for DNA uptake

Vibrio cholerae

(Meibom, Blokesch et al. 2005)

Various stress conditions

Competence for DNA uptake

Gram-positive bacteria

(Claverys, Prudhomme et al. 2006)

DNA damage

Recombination and mutator polymerases (SOS response)

Escherichia coli, Bacillus subtilis and other bacteria

(Sutton, Smith et al. 2000; Au, Kuester-Schoeck et al. 2005)

DNA damage

Prophage excision

E. coli, B. subtilis and other bacteria

(Goranov, Kuester-Schoeck et al. 2006; Rokney, Kobiler et al. 2008).

DNA damage

Horizontal transfer of integrated conjugative (ICE) elements

Multiple bacteria

(Beaber, Hochhut et al. 2004; Auchtung, Lee et al. 2005).

DNA damage

ISDra2 transposition

Deinococcus radiodurans

(Pasternak, Ton-Hoang et al. 2010)

DNA damage

Genetic exchange

Helicobacter pylori

(Dorer, Fero et al. 2010)

UV irradiation

Tn10 transposition

E. coli

(Eichenbaum and Livneh 1998)

Oxidative stress

SOS responses, prophage induction

Multiple bacteria

(Giuliodori, Gualerzi et al. 2007; Selva, Viana et al. 2009)

Chemical damage

SOS response

E. coli, Salmonella typhimurium

(Mersch-Sundermann, Mochayedi et al. 1993; Mersch-Sundermann, Rosenkranz et al. 1994; Mersch-Sundermann, Schneider et al. 1994)

Antibiotic

SOS response

E. coli

(Phillips, Culebras et al. 1987; Miller, Thomsen et al. 2004)

Antibiotic

Competence for DNA uptake

Staphylococcus aureus

(Prudhomme, Attaiech et al. 2006)

Antibiotic

Prophage excision

Staphylococcus aureus

(Goerke, Köller et al. 2006)

Antibiotic (beta lactam)

SOS response and horizontal DNA transfer

Staphylococcus aureus

(Maiques, Ubeda et al. 2006)

Antibiotic

Mutator polymerase

E. coli

(Pérez-Capilla, Baquero et al. 2005)

Tetracycline

CTnDOT excision and conjugal transfer

Bacteroides sp.

(Moon, Shoemaker et al. 2005)

Quorum pheromones, plant metabolites (opines)

Conjugal transfer

Agrobacterium tumefaciens

(Fuqua and Winans 1994)

Plant phenolics

T-DNA transfer to plant cell

A. tumefaciens

 (Gelvin 2006)

Magnetic fields

Tn5 transposition

E. coli

(Chow and Tung 2000)

Magnetic fields

Tn10 transposition

E. coli

(Del Re, Garoia et al. 2003; Del Re, Bersani et al. 2004)

Heat shock

F plasmid transfer

E. coli

(Zahrl, Wagner et al. 2007)

Growth phase

F plasmid transfer

E. coli

(Will, Lu et al. 2004)

Genome reduction

Stress-induced IS elements

E. coli

(Posfai, Plunkett et al. 2006)

Conjugation

ISPst9 transposition

P. stutzeri

(Christie-Oleza, Lanfranconi et al. 2009)

Sex pheromones

Conjugation agglutinins

Enterobacter fecaelis

(Kozlowicz, Dworkin et al. 2006; Kozlowicz, Shi et al. 2006; Clewell 2007; Dunny 2007)

Nucleic acid precursors

Reduce competence

Haemophilus influenzae

(MacFadyen, Chen et al. 2001)

Aerobic starvation

Mu prophage activation

E. coli

(Maenhaut-Michel and Shapiro 1994) (Lamrani, Ranquet et al. 1999)

Stringent response (starvation-induced ppGpp synthesis)

Activation of IS element transcription and IS3 transposition

Caulobacter crescentus

(Boutte and Crosson 2011)

Aerobic starvation

Tn4652 activation

Pseudomonas putida

(Horak, Ilves et al. 2004; Ilves, Horak et al. 2004)

Aerobic starvation

Base substitutions

E. coli

(Bjedov, Tenaillon et al. 2003)

Aerobic starvation

Tandem duplications and amplifications

Salmonella enterica

(Kugelberg, Kofoid et al. 2006)

Aerobic starvation

Plasmid transfer and replication

E. coli

(Peters and Benson 1995; Peters, Bartoszyk et al. 1996)

Elevated temperature

IS element activation

Burkholderia sp.

(Taghavi, Mergeay et al. 1997; Ohtsubo, Genka et al. 2005)

Elevated temperature and high culture density

IS4Bsu1 element

B. subtilis

(Takahashi, Sekine et al. 2007)

Adenine starvation

Ty1 retrotransposon activation

Saccharomyces cerevisiaea

(Todeschini, Morillon et al. 2005) (Servant, Pennetier et al. 2008)

DNA damage (radiation or carcinogen)

Ty1 retrotransposon activation

S. cerevisiaea

 (Bradshaw and McEntee 1989; Sacerdot, Mercier et al. 2005; Stoycheva, Massardo et al. 2007)

Telomere erosion

Ty1 retrotransposon activation

S. cerevisiaea

(Scholes, Kenny et al. 2003)

MAPK cascade activation during filamentous growth

Ty1 retrotransposon activation

S. cerevisiaea

(Conte and Curcio 2000; Morillon, Springer et al. 2000)

Oxidative conditions (H2O2) mediated by SREBP trancription factor

Tf2 retrotransposon activation

Schizosaccharomyces pombe

(Sehgal, Lee et al. 2007)

Mating pheromone

Ty3 retrotransposon activation

S. cerevisiaea

(Kinsey and Sandmeyer 1995)

Mating pheromone

Ty5 retrotransposon activity and transcription

S. cerevisiaea

 (Ke, Irwin et al. 1997)

Prion formation

Genome instability

S. cerevisaea

 (True and Lindquist 2000)

Improper cryopreservation

Ty1 retrotransposition

S. cerevisaea

 (Stamenova, Dimitrov et al. 2008)

Nitrogen starvation

LTR retrotransposon transcription

Diatom (P. tricornutum)

 (Maumus, Allen et al. 2009)

Aldehyde (decadienal) treatment

LTR retrotransposon transcription

Diatom (P. tricornutum)

 (Maumus, Allen et al. 2009)

DNA damage (Mitomycin C)

Transposon and retrotransposon activation

Drosophila melanogaster

(Georgiev, Korochkina et al. 1990)

DNA damage

Alu retransposition

Homo sapiens

 (Hagan, Sheffield et al. 2003)

Gamma irradiation

LINE-1 retrtransposition

Homo sapiens (human osteosarcoma cells)

(Farkash, Kao et al. 2006)

Benzpyrene

LINE-1 retrotransposition

Homo sapiens  (HeLa cells)

(Stribinskis and Ramos 2006)

Steroid hormones

Mouse mammary tumor virus (MMTV) activation

Mus musculus

(Truss, Chalepakis et al. 1992)

Plant alarm chemicals

Retrotransposon activation

Nicotiana tabacum

(Beguiristain, Grandbastien et al. 2001)

Free radical-generating agents, UVC or rose Bengal (RB)

Increased homologous recombination, systemically transmitted

Tobacco

 (Filkowski, Yeoman et al. 2004)

Hydrostatic pressure

MITE DNA transposons

rice

(Lin, Long et al. 2006)

Cutting/wounding

Retrotransposon activation

N. tabacum

(Sugimoto, Takeda et al. 2000)

Protoplasting & growth in tissue culture

Transposon and retrotransposon activation

various plants

(Hirochika 1993; Huang, Zhang et al. 2009)

Protoplasting & growth in tissue culture

Tos17 retrotransposon activation

rice

 (Hirochika, Sugimoto et al. 1996)

Growth in tissue culture

mPing transposition

rice

 (Ngezahayo, Xu et al. 2009)

Cell culture growth

1731 LTR retrotransposon

D. melanogaster

(Maisonhaute, Ogereau et al. 2007)

Cell culture growth

LINE-1 element retrotransposition

Mouse cell line

(Moran, Holmes et al. 1996)

Fungal metabolites

TnT1 retrotransposon

Nicotiana tabacum

(Melayah, Bonnivard et al. 2001)

Chlorine ions (not sodium)

DNA strand breaks and recombination

Arabidopsis thaliana

(Boyko, Hudson et al. 2006; Boyko, Golubov et al. 2010)

Nickel, Cadmium and other heavy metals

LINE-1 retrotransposition

Homo sapiens tissue culture cells

(El-Sawy, Kale et al. 2005; Kale, Moore et al. 2005; Kale, Carmichael et al. 2006)

Temperature and day length

 

Homologou recombination

 

Arabidopsis thaliana

(Boyko, Filkowski et al. 2005)

Helicobacter pylori infection

Adenocarcinoma with microsatellite instability

human gastric mucosa

 (Tahara 2004) (Li, Shi et al. 2005) (Moriichi, Watari et al. 2009)

Fungal or virus infection

(CT)n microsatellite contraction

wheat

(Schmidt and Mitter 2004) (Kovalchuk, Tryndyak et al. 2007)

Barley stripe mosaic virus (Peronospora parasitica) infection

Increased somatic recombination and transposon activation; transmissible systemic response in tobacco

Arabidopsis, maize and tobacco

 (Kovalchuk, Kovalchuk et al. 2003)

Tobacco mosaic virus and oilseed rape mosaic virus infection

Increased somatic recombination (transmissible systemic response)

Tobacco, Arabidopsis thaliana

 (Dong 2004; Boyko, Kathiria et al. 2007)

Temperature

Amplification/reduction in repetitive elements

Festuca arundinacea (Tall Fescue)

(Ceccarelli, Esposto et al. 2002)

Elevation and moisture

BARE-1 retrotransposition

Hordeum spontaneum (wild barley)

(Kalendar, Tanskanen et al. 2000)

Heat shock, toxic chemicals

SINE transcription

Bombyx morii

(Kimura, Choudary et al. 1999; Kimura, Choudary et al. 2001)

Various stress conditions

SINE transcription

H. sapiens

(Li and Schmid 2001)

Heat shock

B1 SINE transcription

M. musculus

(Li, Spearow et al. 1999)

Industrial air pollution

Microsatellite expansion

M. musculus

(Somers, Yauk et al. 2002)

Particulate air pollution

Germ-line mutations

Mouse

(Yauk, Polyzos et al. 2008)

Chemical mutagens and etoposide

Microsatellite expansion

M. musculus

(Vilarino-Guell, Smith et al. 2003)

Diet (extra folic acid, vitamin B12 choline, and betaine)

IAP retrotransposon at Agouti locus (Avy allele)

M. musculus

(Waterland and Jirtle 2003)

Lymphocyte differentiation and antigen activation

Activation of VDJ joining, somatic hypermutation and heavy chain class switching

M. musculus and H. sapiens

(Gellert 1997; Honjo, Kinoshita et al. 2002; Alt 2007)

Neuronal differentiation and exercise

LINE-1 retrotransposition

M. musculus

(Muotri, Chu et al. 2005; Muotri, Zhao et al. 2009); (Coufal, Garcia-Perez et al. 2009)

Hybrid dysgenesis

P factor transposon

D. melanogaster

 (Kidwell 1985; Kidwell, Kimura et al. 1988) (Kocur, Drier et al. 1986)

Hybrid dysgenesis

I factor non-LTR retrotransposon

D. melanogaster

(Fawcett, Lister et al. 1986; Bucheton 1990; Busseau, Chaboissier et al. 1994; Sezutsu, Nitasaka et al. 1995; de La Roche Saint Andre and Bregliano 1998; Gauthier, Tatout et al. 2000)

Hybrid dysgenesis

Hobo transposon

D. melanogaster

(Yannopoulos, Stamatis et al. 1987) (Simmons 1992) (Galindo, Ladeveze et al. 1995; Bazin, Denis et al. 1999; Bazin, Dejonghe et al. 2004)

Hybrid dysgenesis

Penelope retrotransposon and other transposable elements

D. virilis

(Scheinker, Lozovskaya et al. 1990; Zelentsova, Poluectova et al. 1999; Evgen'ev, Zelentsova et al. 2000; Lyozin, Makarova et al. 2001; Pyatkov, Shostak et al. 2002; Blumenstiel and Hartl 2005; Evgen'ev and Arkhipova 2005)

Hybrid dysgenesis

Mariner/Tc1, hAT transposons and gypsy/Ty3 LTR retrotransposons

Medfly (Ceratitis capitata)

(Torti, Gomulski et al. 1997; Gomulski, Torti et al. 2004)

 

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