Taxonomic and Developmental Aspects of Radiosensitivity

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Taxonomic and Developmental Aspects of Radiosensitivity

F.L. Harrison

S.L. Anderson

This paper was prepared for submittal to the

Symposia on Ionizing Radiation

Stockholm Sweden

May 20-24 1996


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DISCLAIMER

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University of California nor any of their employees, makes any warranty, express

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imply its endorsement, recommendation, or favoring by the United States

Gove rnmen t or the University of California. The views and opinio ns of authors

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TAXONO MIC A ND DEVELOPMENTAL ASPECTS OF RADIOSENSITIVITY

Florence L Harrison 1 and Susan L And erson ^

1 Lawrence Livermore National Laboratory, Livermore, CA 94550

2 Lawrence Berkeley National Laboratory, Berkeley, CA 94720

Abstract

Considerable information is available on the effects of radioactivity on adult and

early life stages of organisms. The preponderance of data is on mortality after a

single irradiation with relatively high doses. Unfortunately, because experiments

were carried out under different conditions and for different time periods, the

validity of comparing the results from different taxonomic groups is questionable.

In general, the conclusions are that there is a relationship (1) between

radioresistance to high doses of acute radiation and taxonomy of the organism,

primitive forms being more radioresistant than complex vertebrates and (2)

between radiosensitivity and developmental stage, early life stages being more

sensitive than later stages. The first conclusion may be related to the capability of

the organism to repopulate cells and to dedifferentiate and redifferentiate them;

the second to the rate of cellular division and to the degree of differentiation. In

question, however, is the relevance of the responses from high levels of acute

radiation to that of the responses to long-term exposure to low levels of radiation,

which are ecologically of more interest. Data from studies of the effects of acute and

chronic exposure on development of gametes and zygotes indicate that, for some

fishes and invertebrates, responses at the cellular and molecular levels show effect

levels comparable to those observed in some mammals. Acute doses between 0.05

and 0.5 Gy and dose rates between 0.02 to 0.2 mG y/h appear to define critical ranges

in which detrimental effects on fertility are first observed in a variety of


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organisms and not just humans, because the stability of ecosystems is vital for

maintenance of the quality of human life. With information available on

responses to irradiation and factors affecting radiosensitivity, organisms in

ecosystems potentially at risk from accidental or planned releases of radioactivity

can be identified. We will review the extensive database on mortality to ascertain

the relationship between radiosensitivity and taxonomy and the less extensive

database on responses of reproductive tissues and early life stages to define the

relationship between radiosensitivity and development.

Abbreviations: Gy, gray; ppt, parts per thousa nd

Taxonomic Aspects of Radiosensitivity

Information is available on the effects of radiation on adult and early stages of

organisms from different phyla and from different types of ecosystems. Although

extensive data are available, there are entire phyla and groups within phyla for

which there is no information; previous studies focused on a few species of

mammals or of fishes. Most of the experiments were conducted to determine the

responses to acute, high doses rather than chronic, low doses. However, it is the

latter type of exposure that is more relevant to conditions that are present currently

in the environment.

Acute Radiation Responses. A common experimental procedure in the past

was to expose test organ isms to a single irradiation usin g a relatively hig h d ose to

determine the dose at which mortali ty occurred. The response to the irradiation


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The effects of acute radiation were examined using many fish species (Table

2). The range of lethal levels is from about 3.75 to 100 Gy. For some fishes, the

effects for a specific total dos e of dec reasin g the dose rate a nd of fractionating the

dose were studie d [17-20]. The results are sim ilar to th ose for m am m als. A s th e

dose rates are decreased and the intervals between fractionated doses are increased,

a greater total


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1 0 -

7

2.5

1.5-

>600

->22

3-40

5-20

-150

>130

Table

1.

Summ ary showing ranges

of

LD50S obta ined from acute irrad iation

of

organism s from different taxonom ic gro ups. 1

Gro up Dose, Gy

Protista 30

-

30,000

Inve rtebra tes 2.1 -1,100

Vertebrates

Fishes

A m p h i b i a n s

Reptiles

Birds

M a m m a l s

Plants

1 The radiation units in references were conv erted to grays for comparat ive

purposes andfor some values are approximations.

doseisrequiredtopro duc e the sam e biological effects observedathigh dose rates


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Table 2. LD50S from acute irradiation of m am mals and fishes. 1

Dose, Gy References

[8-10]

[in

[12]

[13]

[14]

[15]

[16]

1 T h e r a d i a t i o n u n i t s i n t h e r e f e r e n c e s we r e c o n v e r t e d t o g r a y s f o r c o m p a r a t i v e

M a m m a l s

H u m a n s

M o n k e y

Dog

S w i n e

H a m s t e r

M o u s e

Rabbi t

Bat

Pisces

Goldfish

M u m m i c h o g

Tench

Guppy

Chinook salmon

Mosquitofish

Pinfish

3

6

2.5

2.5

6

6.4

7.5

150

3.75 -100

10-20

12-55

23.5

25

37

50


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n

the


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Table3 . LD50S obta ined f rom acu te i r r ad ia t ion of inver t e bra te org ani s m s f rom

d i f fe ren t

t a x o n o m i c

g r o u p s .

G r o u p

Dose ,G y Ref e r ences

[21]

[22]

[ ]

[ ]

[ 3]

[24]

[25,26]

[ 7 8]

[ 5]

1 The radiation units provided in references were converted to grays for

comparative purposes and for some values are approximations. Also, the exposure

times in some experiments differed from 30 days.

Protozoa

Coelenterata

Porifera

Adul t

P la tyhelminthes

Anne l ida

Adult

Mollusca

Early life

Adul t

Crustacea

Adult

Echinodermata

>1000

20 -120

20 -120

55

100 - >500

11

50 - 500

2.1 -10 00

100


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quantified by observing changes in the number and condition of primordial germ

c e l l s and


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Figure 1

For the same LD50 value, the shape of species response curves from

radiation may differ significantly.

developing gametes or in the size of the gonad. They may be quantified also by

observing changes in the number of fer t i l ized eggs produced and in the

morphology and physiology of the developing embryos. When early life stages are

irradiated, the effects quantified include the induction of abnormalit ies in the

embryos and increases in mortality. Although the database is far from complete,

sufficient information is available to permit some comparisons to be made.

An exam ple of changes in sensitivity am ong d eve lopm enta l s tages is

available from th e wor k of Ravera [26] wh o show ed LD50 valu es for the four-cell,


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Acute Radiation Responses. Acu te irradiatio n of repro duc tive tissues and

early life stages results in changes in fertility, sterility, and normal development.

T h e range


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Table 4 . Ch ang es in the r ad iosens i t iv i ty of r a in bo w t rou t Salmo gairdnerii e x p o s e d

to acu te i r r ad ia t ion d ur in g de ve l op me nt [14, 38 ] . 1

Sta ge in life cycle LD50 (Gy)

G a m e t e 0 . 5 - 1 . 0

1 cell 0.58

32 cell 3.1

Ge rm r in g 4.5 - 4.6

Eyed 4.1 - 9.0

A d u l t 1 5

1 The rad ia t ion uni t s in r e fe rences we re conve r ted to grays for compara t ive

p u r p o s e s . 1

Table 5. Sens i t iv i ty of d i f f e ren t end po in t s in the po lyc hae te w or m Neanthes

arenaceodentata.

Dose , Gy

>0.3

E n d p o i n t

D N A - s t r a n d b r e a k a g e

References

[39]


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germ cells were observed after exposures to doses of acute radiation as low as 2.5

Gy. Welander et al.[14] found that co unts of pr imo rdial germ cells in the Chinoo k

salmon Oncorhynchus tschawytscha exposed to 2.5 Gy from a x-ray source we re

10% of control values. Male germ cells of the medaka Oryzias latipeswere studied

extens ively by Egami and co-workers , who found a temporary reduct ion in

testicular weig hts after e xpo sure to a range from a bou t 1 to 20 Gy.

In fishes, irradiation not only may retard development but also alter

morphological and physiological characteris tics . Some of the criteria used to

evaluate effects include hatching success, embryo mortali ty, and frequency of

morphological abnormalities in embryos, larvae, young, and adults [32,33]. Other

responses noted were tha t the somatic damage in Chinook sa lmon was

proportional to the amount of radiation received and that the greatest amount of

damage was in t issues growing and dividing rapidly. From the differences in

sensitivit ies shown by successive early stages of development, i t appears that

different processes are involved and that these processes are in progress at various

times prior to morphological evidence of the organogenesis.

Chronic Radiation Responses. Dose rates that resulte d in significant

changes to fertility in invertebrates had a larger range of values than in fishes and

mammals; the range for the invertebrates was from 0.07 to 550, for fishes


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p o l y c h a e t e w o r m

Neanthes


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Table 6 . Co mp ar i son o f sens i t iv i ty of rep rod uc t ive t i s sues of in ver t eb ra tes , f i shes ,

and m am m als ex pose d to acu te i r rad ia t i on (Gy) . The doses for fe rt i li ty a re those a t

which s ign i f ican t changes were no ted and fo r s te r i l i ty were fo r when the response

wa s no ted . 1

Fertil ity Steril ity References

Invertebrates

Neanthes arenaceodentata

( p o ly c h a e t e wo r m , a d u l t s )

Gammarus duebeni

( a m p h ip o d , a d u l t s )

Artemia salina

( b r in e s h r im p , j u v e n i l e s )

Diaptomus davipes

( c o p e p o d , e m b r y o s )

Crepidula fornicata

( s l ipper l impe t , l a rvae)

Physa acuta

( f reshwate r sna i l , adu l t s )

Fishes

Oryzias latipes

( m e d a k a , a d u l t m a le s )

0.5

2.2

9

10

20

20

5

50

21

1000

[23]

[31]

[42]

[43]

[44]

[26,45]

[46]


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Table 7. Comparison of sensitivity of reproductive tissues of invertebrates, fishes,

and m am mals exposed chronically to radiation ( m G y/ h) . The doses for fertility are

those at which significant changes were noted and for sterility were for when the

response was noted. 1

Invertebrates ertility Sterility References

Pollicipes polymerus

0.07 [50]

goosebarnacle, larvae)

Neanthes

arenaceodentata

0.19 20 [51]

( w o r m , s i n g l e g e n e r a t i o n )

Ophyrotrocha diadema

3.2 [52]

( w o r m , s e v e n g e n e r a t i o n s )

Daphnia pulex

550 1400 [36]

(wa te r f l e a , mul t ip le gene ra t ions )

F i s h e s

Ameca splendens


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arenaceodentata, the difference is two orders of magnitude whereas for male dogs

it is a factor of abo ut tw o.

Reproductive success for a given species may be related not only to its

sensitivity to radiation during gametogenesis and early development but also i ts

reproductive strategy [32, 33]. For exam ple, in a high ly fecund species, the surviva l

of early life stages may be very low, and the loss of abnormal embryos induced

from radiation expo sure may be mask ed completely by those lost from other

ecological factors, such as food limitation and predation. Other important factors of

reproductive strategy, in addition to the total number of gametes produced, their

rate of division, and their sensitivity, are gametogenesis parameters, such as the

time between production and release of gametes, the time to sexual maturity, and

the brooding of young. The time between the formation of primary germ cells and

the release of mature gametes becomes important in long-lived species exposed to

chronic irradiation. In the case of marine mammals and some fishes, if repair of

radia t ion damage does not occur , the dose to reproduct ive t issues may be

integrated over a period of tens of years . Unfortunately, in man y non ma m mia n

organisms the processes involved in radiosensitivity and in gametogenesis and

reproductive strategies are not known.

The data most relevant to protection of ecosystems through limit setting are

those values obta ined from developmenta l responses ra ther than morta l i ty

because high radiosensitivity of gonadal t issues and early l ife s tages affects

reproductive success directly. Also, if for the same group of species the


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information from only a few studies that were on multigenerations. The duration

of most studies was for less than a complete life cycle, and the stages in the life cycle

irradiated were not always comparable. The database from field studies includes

results from multigeneration investigations, but the results from many of these

studies were confounded by the presence in the ecosystem of con taminants other

than radioactivity [6]. Effects of multigeneration exposu re becomes imp ortant

because the dose-response curves for specific species may differ greatly (see Fig. 1). It

can be expected that selection of radioresistant individuals will occur upon

continuous exposure, and species having a broader range in sensitivity may have a

greater potential for survival.

Inherent Radiosensitivity Factors

The information reviewed indicates that responses during reproduction and

development, which may reflect changes at cellular and molecular levels,

represent better the inherent radiosensitivity of the species than the mortality

responses of adults. We will consider inherent radiosensitivity factors to be those

that are controlled by the genetic make up of the organism and that determine

basic developmental processes and pathways as well as biological repair processes.

Although environmental conditions, such as temperature, salinity, contaminants,

and exposure conditions, are known to alter the observed radiosensitivity, there

are some parameters that most likely reflect inherent radiosensitivity of an

organism. Such parameters include the (1) nuclear material content, (2) cell


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sensitivity of plants to chronic irradiation. Additional work on INV and sensitivity

was performed on amphibians, where a similar relationship was determined [7].

Cell Repopulation. The ability of cells to repo pula te them selves to replace

cells damaged by injury or by radiation and to orchestrate t issue and organ

regeneration is undoubtedly an inherent trait of organisms. In t issue repair, a

number of growth-factor genes are induced and help direct tissue repair, but the

molecular signals that initiate the process are not established completly but are

currently un de r investigation [58]. The cells involved in repo pulatio n an d division

may be cells that never differentiated, such as primordial germ cells, stems cells,

and othe r type s of cells that were set aside du rin g early dev elop m ent [59], or cells

that ha d dedifferen tiated or transd ifferen tiated [60]. If orga nism s hav e the capacity

to replace cells, the radiation damage observed at the whole organism level may be

masked.

Tissue and Organ Regeneration. Tissue and organ regeneration has been

demonstrated in many more primitive organisms, some of which appear to be

relatively radioresistant as adults. The ability of cells to repopulate is undoubtedly

an important component of regeneration. Both the abilities to repopulate cells and

regenerate s tructures are related to basic developmental processes and pathways

and are important components of recovery from radiation damage.

The m etho ds of cell specialization by em bryos from different phylog enetic

grou ps w ere s tudied and sho wn to be diverse [61]. But no w s tud ies of

developmental processes and pathways appear to be entering a crucial period of


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are they known to play a role in sporulation in B. subtilus but also in cell fate in

the algae Volvox carteriand in the develop me nt of the nervou s system of the fruit

fly [63]. H ow eve r, ultim ate differences in the cells m ust d ep en d o n the activation of

distinct genes in each cell. Differential activation is considered to be accomplished

through a series of transcriptional factors called sigma factors. These sigma factors

are proteins reported to bind to s ites near the beginning of genes to init iate

messenger RNA synthesis . The abili ty to produce signaling proteins and sigma

factors du rin g early life and ad ult stages may accou nt in par t for differences am ong

organisms in their capabili t ies to repopulate damaged cells and to regenerate

tissues and organs.

Biological Repair. Inherent radiosensitivity is also related to the biological

repair capability of cells. Biological repair consists of repair of nuclear as well as

cytoplasmic materials. The main focus of repair in the nucleus is on the processes

involved in the repair of DNA; that of cellular repair is on the group of enzymes

that are involved in the prevention of and in the repair of damag ed constituents

within the cytoplasm.

The ability of cells to repair radiation damage was noted early on when

organisms were observed to often show reduced sensitivity when exposed to

fractionated doses [ 1, 32, 33]. The conc lusion wa s m ad e th at sp litting the dos e

allows repair processes to reduce the damage. Currently, there is sufficient

information to conclude that repair mechanisms are widely distributed and are

impo rtant to radiosens i tiv i ty responses . The mec hanism receiving the mo st


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documented that treatment of dividing cells with radiation causes a pause in the

G2 phase of the cell cycle, and wh en the paus e is absent, the cells are mo re sensitiv e

to radiation. Recently, many proteins in the checkpoint pathways were identified

in yeast [68, 69]. Mitotic check points req uire three distinct functions: (1) a detection

system to determine the change in DNA structure, (2) a signal pathway to transmit

this information, and (3) an effector mechanism to interact with the cell-cycle

machinery. It is expected that the p rogress m ade in the genetic analysis of yeast w ill

yield identification of biochemical markers for checkpoints, which can be used to

characterize responses in other organisms.

Indirect damage in genetic material from free radicals produced in cells

from radia tion is a likely occurrence [32, 33]. Defense m echa nism s ag ainst the

production of free radicals formation were reviewed by Giulio et al. [70] who were

concerned primarily about xenobiotic molecules, such as quinone, aromatic nitro

compounds, aromatic hydroxylamines, bipyridyls, and certain metal chelates. They

prop osed that antioxidant defenses are of three general classes and include water

soluble reduc tants (glutathione, ascorbate, urate), fat soluble v itam ins (alpha

tacopherol , be ta carotene) and enzymes (gluta thione peroxidase , ca ta lase ,

supero xide dism utase). The enzym es are of special interest because they are

inducible under conditions of oxidative stress.

Much of the indirect damage caused by ionizing radiation is considered to

be due to the hydroxyl radical, which is one of the most reactive radical known. In

the presence of transition metal catalysts, superoxide and hydrogen peroxide will


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invertebrates, some information is available on methods to quantify oxidative

stress-related responses induced in these organisms from xenobiotic chemicals [70].

Adaptive R esponses to Low Levels of Radiation

M ore a t t en t ion has bee n d i r ec ted recent ly to r espo nses to low l evel s of r ad ia t io n

and w h a t ha s been ca ll ed an adap t i ve r e sponse . Th i s r e spon se to l ow doses ,

which r emains for severa l hour s in mammals , i s somet imes r efer r ed to as s t r ess

resp on se or res po nse to geno toxic st ress, an d it m ay affect ou r use of the l in ear- no -

t h r e s h o l d t h e o r y f o r r a d i a t i o n d a m a g e . C o n s i d e r a b l e d a t a h a v e a c c u m u l a t e d

indicat ing that low doses of radiat ion may resul t in changes in the cel ls , ref lect ing

an ab ili ty to ada pt to th e effects of rad iati on [6, 32, 33]. In the UN SC EA R re po rt [4], i t

i s no ted th at the con ven t iona l est i ma tes of the r isks of stoch ast ic effects of low

doses of ioniz ing r adia t ion many have been over s t a t ed because no a l lowance was

made for the adapt ive r esponse .

Repor ted mani fes t a t ions of adapt ive r esponses in mammals a re acce lera t ed

g r ow t h , i nc r eased r e p r o du c t i ve ab i l it y , ex t e nde d l if e spa n , s t i m u l a t i on o f t he

i m m u n e s y s t e m , a n d r e d u c e d i n c id e n c e of r a d i a t i o n - i n d u c e d c h r o m o s o m a l

abe r r a t i ons and m u t a t i ons . Som e o f t he m echan i sm s p r oposed t o be i nvo l ved i n

the adapt ive r esponse and might be expected to be r ef l ec ted in r ad iosens i t iv i ty

responses were the fol lowing [4] :

( a) the ef fec ts of r ad ia t io n on the up - reg ula t ion of gen es an d the i r

inf luence on cel l cycle kinet ics;


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bivalve and a polychaete worm [39]. Results from experiments using DNA-strand

breakage as the endpoint indicate that after these organisms are irradiated, DNA-

strand breakage is repaired. However, the time course of repair is much slower in

nonmammals than mammals; the time of repair takes days rather than hours.

Also, little is known about the fidelity of the repair. Another important

consideration is that in mammals there is evidence that the lesions induced by

radiation may also be induced by some other toxic agents. These not only include

physical agents bu t also chemical materials. Before the consequence of low doses of

radiation on nonmammalian species can be elucidated, allowance for uncertainty

should be considered in predictions of effects on the environment. The adaptive

response and its effect on interactions amo ng contam inants in the environ ment

becomes a research area that needs to be addressed.

Summary

The ranges of the LD50 responses of different taxonomic grou ps of organisms to

acute radiation indicate that there are large differences among groups in

radiosensitivity and that lower taxonomic groups have lower radiosensitivity. Lists

of median lethal doses causing mortality are to be interpreted with caution when

making comparisons about radiosensitivity of specific species within a group and,

in some cases, of species from different phyla. Also, because the responses that are

elicited at high doses may be entirely different from those at low doses, erroneous

conclusions may be drawn when short-term mortality results are used to


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The inherent radiosensitivity, which is genetically controlled in an

organism, is a crit ical factor in determining the responses to radiation. The

responses observed may be modified by environmental factors and physiological

condition but reflect fundamental processes and pathways in reproduction and

development and the ability to prevent or repair damage to biologically critical

molecules. Even though deleterious responses are not detected generally above the

apparent lower threshold level, effects may be occurring that cannot be quantified

with our current state of technology. Because rapid process is being made in the

understanding of developmental processes and pathways and in biological repair

mechan isms, information may be available soon that will allow us to u nde rstand

factors de termining inherent radiosens i t iv i ty and to ident i fy endpoints or

biom arkers to be used to set better stan dar ds for the protection of hum ans and the

e n v i ro n m e n t .


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Acknowledgements :

Work performed under the auspices of the U.S. Department of Energy by Lawrence

Livermore National Laboratory under Contract No. W-7405-Eng-48.


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University of California Live rmore, California 94551

Taxonomic and Developmental Aspects of Radiosensitivity

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